Oral Surgery ISSN 1752-2471

ORIGINAL ARTICLE

Deep peri-implantitis: two cases treated with implant apicoectomy

with follow-up of at least 7 years
D. Kalyvas1, M. Tarenidou1, G. Zorogiannidis2, E. Tsetsenekou1 & A. Grous3
1

Oral Surgery, Dental School, Oral and Maxillofacial Surgery, University of Athens, Athens, Greece
General private practitioner, Athens, Greece
3
Private Prosthodontist, Athens, Greece
2

Key words:
implant apicoectomy, peri-implantitis,
radiolucency
Correspondence to:
Professor D Kalyvas
Oral Surgery
Dental School
Oral and Maxillofacial Surgery
University of Athens
str. Thivon 2, Goudi
11567 Athens
Greece
Tel.: + 0030-210-8233608
email: demkal@dent.uoa.gr
Accepted: 21 October 2014
doi:10.1111/ors.12140

Abstract
Aim: Deep periimplantitis is a lesion located in the periapical region of an
osseointegtated implant. The aim of this study was to present 2 cases of this
feature treated with apicoectomy.
Materials and methods: Two cases of deep periimplantitis located in the
maxillary premolar region are presented in this report. Both the lesions
were situated in the apical segment of otherwise osseointegrated and long
(15 mm) implants. They were treated with surgical debridement,
apicoectomy, bone substitute and antibiotics.
Results: Bone overheating, proximity to periapical lesions or previous
inflammation seem to be the three possible causes of the lesions in the cases
presented. The follow-up period of 7 and 10 years indicates that implant
apicoectomy is a safe and reliable treatment choice.
Conclusions: The treatment of choice for deep periimplantitis is implant
apicoectomy, unless the implant is mobile, where implant removal is
preferable.

Clinical relevance

apex resection with a follow-up period of 7 and 10

years.

Scientic rationale for study

Deep peri-implantitis is a lesion defined as a bone loss
limited to the apical segment of an otherwise
osseointegrated implant. The radiolucent lesion
usually appears shortly after implant insertion and is
accompanied by symptoms of pain, tenderness,
swelling and/or the presence of a fistulous tract. The
aetiology and mechanism of this lesion are multifactorial. Most commonly, factors such as bone overheating or periapical inflammation of, either an
adjacent tooth, or a previously extracted tooth at the
implant site, are implicated. Several methods have
been proposed to treat deep peri-implantitis. Among
these, implant apicoectomy seems to be an effective
treatment with long-term results and few complications, if any. The aim of this article is to present two
cases of deep peri-implantitis treated with implant
200

Principal ndings
It is noted that in both cases, the maxillary premolar
region is involved. Additionally, both the affected
implants were 15 mm long, which suggests that a possible cause of deep peri-implantitis in these cases was
bone overheating during implant placement. However,
in the first case, there is no dental record for the
extracted tooth 15 and, therefore, the remaining
inflammatory cells or bacteria from a periapical lesion
cannot be excluded as a possible cause. As far as the
second case is concerned, the lesion can also be attributed to the fact that the implant at site 14 was placed in
close proximity to the root of tooth 13 and its periapical
lesion.
The peri-implantitis in both cases was treated with
amoxicillin 500 mg 3 6, surgical debridement,
Oral Surgery 8 (2015) 200--207.
2014 The British Association of Oral Surgeons and John Wiley & Sons Ltd

Deep peri-implantitis

Kalyvas et al.

apicoectomy and use of bone substitute. During the 7

years and 10 years follow-up period, there are no
clinical signs, symptoms or radiographic findings.

Practical implications
In order to treat deep peri-implantitis, several
approaches have been proposed. They include surgical
debridement (curettage), implant detoxification,
guided tissue regeneration, apical resection and
implant removal. Undoubtedly, implant removal is the
preferable treatment for mobile implants. Implant
apicoectomy appears to be an effective treatment
method. The uncomplicated follow-up period of 7 and
10 years points out this approach as a treatment of
choice.

Introduction
Deep peri-implantitis is a lesion defined as a bone
loss limited to the apical segment of an otherwise
osseointegrated implant. Other terms used to
describe this lesion are localized osteomyelitis1,
endodontic implantitis2, apical periimplantitis3,4,
periapical implant lesion512, retrograde periimplantitis1315, periradicular lesion1620 and periapical
radiolucencies21. We believe that the term deep
periimplantitis stands better for the inflammatory
nature and the origin of the lesion. Deep periimplantitis can present as an apical radiolucency
associated with an integrated implant. Accompanying
signs and symptoms can include pain, swelling, tenderness and the presence of a sinus tract (Table 1).
The first cases were described by McAllister et al.21 in
1992 and Sussman and Moss1 in 1993. Reiser and
Nevins (1995)7 defined this complication as implant
periapical lesion and suggested its aetiology, classification (into inactive and infective lesions) and treatment.
Sussman (1998)26 proposed a classification in case types
1 (implant to tooth) and 2 (tooth to implant).
The prevalence of deep peri-implantitis varies
between 0.26% and 1.8%7,14. There is a higher incidence for implants in the maxilla (3:1), and the predominant sites are the maxillary central incisor and
first premolar areas (Table 1)14. Most of the implicated
implants are 12 mm long or more. The overall failure
rate is higher for machined implants. There is one
retrospective study14 reporting a higher incidence of
deep peri-implantitis for TiUnite (Nobel BioCare,
Gteborg, Sweden) implants (8/80) rather than for
machined implants (2/459), but the numbers included
are very small.
Oral Surgery 8 (2015) 200--207.
2014 The British Association of Oral Surgeons and John Wiley & Sons Ltd

The aetiology and mechanism of this lesion are

unknown, and there are many theories as to how the
lesion arises. Most commonly, factors such as bone
overheating or periapical inflammation of, either an
adjacent tooth, or a previously extracted tooth at the
implant site, are implicated. Several methods have
been proposed to treat deep peri-implantitis. Among
these, implant apicoectomy seems to be an effective
treatment with long-term results and few complications, if any. The aim of this article is to present two
cases of deep peri-implantitis treated with implant apex
resection with a follow-up period of 7 and 10 years.

Case report no. 1

A 52-year-old woman with no significant medical
history appeared with a fused-to-metal crown at tooth
14 and a cantilever at the site of the missing tooth 15,
which had been extracted 3 years before. There is no
record for the missing tooth 15 and the reason for its
extraction. The tooth 14 was extracted due to periodontal infection and class 3 mobility. The patient had
two implants placed by drilling at sites 14 and 15 on
July 1999, 5 months after the extraction of the tooth 14
(Fig. 1). The implant type was Lifecore Restore
machined, and their diameter and length were
3.3 11.5 mm and 3.75 15 mm, respectively.
According to our protocol, 1 g of amoxicillin was
administered 1 h preoperatively and for 4 days postoperatively. On August 2000, a fistula was noted
(Fig. 2). There was also mild pain at palpation. Radiographically, there was a radiolucency around the apex
of the implant at site 15 and a gutta-percha cone
inserted in the fistula pointed at the apex of this
implant (Fig. 3). The peri-implantitis was treated with
amoxicillin 500 mg 3 6, surgical debridement,
apicoectomy and use of bone substitute (BioOss
(Geistlich Pharma North America Inc., Princeton, USA)
granules 0.251 mm) (Figs. 46). During the 7 years
follow-up period, there are no clinical signs, symptoms
or radiographic findings (Fig. 7).

Case report no. 2

A 44-year-old man with no significant medical history,
except from the fact that he is a heavy smoker (40
cigarettes/day), appeared with an implant-tooth
retained restoration. After clinical and radiographic
examination, the extraction of implants and teeth
was decided, except from teeth 13 and 27, which
were endodontically treated and used to retain the
provisional restoration. In November 1996, 5 months
after the extractions, he had six Lifecore (Lifecore
201

202

Mohamed et al.18

Kalyvas et al. (2009)

a. 15
b. 14
22

a. 14
b. 24
c. 44
d. 24
45
43
12

Quirynen et al.24

Tseng et al.12
Bousdras et al.25
Tzm et al.8

12
36

Flanagan4
Oh et al.6

a. 24, 25
b. 25
c. 43

Implant site

46, 47
a. 42
b. 46
c. 46
d. 45

13

Chaffee et al.22
Brisman et al.23

Ayangco and Sheridan

Authors

a. 13 months after placement

b. 12 months after placement
4 months

a. 3 months later
b. 3 weeks later
c. 2 weeks later
d. 6 days later
6 months after prosthesis
1 month after prosthesis
5 years after implant placement

10 weeks post-operatively
At uncovery surgery

35 days later
a. 6 weeks later
b. After 4 months and after 4 weeks
c. After 4 months
d. 2 weeks later

a. 18 months after prosthesis

b. 9 months after prosthesis
c. 1 month after

Time of appearance

Table 1 Signs, symptoms and aetiology of deep peri-implantitis

a. Fistula, pain at palpation

b. Pain at percussion
c. Pain, swelling, stula, pus secretion
d. Swelling
Pockets, loss of osseointegration
Pain
7 mm probing depth with pus formation,
periapical stula
a. Fistula, mild pain at palpation
b. Halitosis, stula, mild pain at palpation
None

Pain
a. Fistula
b. Fistula, implant mobility
c.
d. Mild pain at palpation, erythema and
swelling.
Pain
Fistula, implant mobility

a. Swelling, stula
b. Tenderness upon touching
c. Pain

Clinical signs, symptoms

a. Lifecore Restore 3.75 15 mm

b. Lifecore Restore 3.75 15 mm
Not reported

4.0 13 mm Osseotite
Brnemark system
3.75 13 mm
a. 15 mm MkIII
b. 13 mm MkII
c. 13 mm MkII
d. 13 mm MkIII
ITI
3.75 18 mm MkIII

3.25 13 mm
4.25 10 mm
3.3 10 mm
5 10 mm (Root formed implants)

a. Bone overheating (possibly ET 15)

b. EP 13
Proximity to 21 (EP)

endodontic pathology (EP) 11

a. ET 14
b. ET 24
c. ET 44
d. Proximity to 23, EP 25, or ET 24.
Proximity 45 to 44, EP 44

ET 12
Remaining root of 36

EP 45
a. ET 42
b. ET 46 or EP 45
c. Proximity of 46 to 45, EP 45
d. ET 45

a. Extracted tooth (ET) 24

b. ET 25
c. ET 43

a. 4 15 mm
b. 4 13 mm
c. 4 13 mm (Brnemark system
implants)
a.
b.
c.
d.

Aetiology

Implant type

Deep peri-implantitis
Kalyvas et al.

2014 The British Association of Oral Surgeons and John Wiley & Sons Ltd

Oral Surgery 8 (2015) 200--207.

Deep peri-implantitis

Kalyvas et al.

Figure 1 Panoramic X-ray of the rst case.

Figure 3 Gutta-percha cone pointing the apex of the implant.

Figure 2 Clinical aspect of the stula.

Figure 4 Intraoperative aspect of the lesion.

Biomedical, Minnesota, USA) implants placed by drilling in his upper jaw at sites 14, 12, 21, 23, 24 and 26
(Fig. 8). The implants diameter and length were
3.75 15 mm for the sites 14, 12, 21, 23 and
3.75 13 mm for the sites 24, 26. According to our
protocol, 1 g of amoxicillin was administered 1 h
preoperatively and for 4 days post-operatively. In July
1997, the teeth 13 and 27 were extracted. In November
1997, the patient presented with a complaint of halitosis and pain at palpation. Clinical examination
revealed a draining fistula (Figs. 9, 10). The treatment
was amoxicillin 500 mg 3 8, apicoectomy of the
implant at site 14 and tissue regeneration with BioOss
and Guidor (Sunstar Americas, Chicago, USA) membrane (Fig. 11). During the 10 years follow-up period,
there are no clinical signs, symptoms or radiographic
findings (Fig. 12).
Oral Surgery 8 (2015) 200--207.
2014 The British Association of Oral Surgeons and John Wiley & Sons Ltd

Discussion
The most frequent sites of deep peri-implantitis commonly appears are adjacent to sites of endodontic
pathology or the extraction sites of endodontically
treated teeth.
The aetiology of the lesion remains unclear. There
are a number of theories that have been presented in
the literature, including bone necrosis following overheating during surgical procedure, translocation of
bacteria from adjacent teeth, undiagnosed pathology at
the extraction sites (remaining inflammatory cells,
granuloma, presence of residual root fragments, fenestration of the vestibular alveolar bone, proximity to an
infected maxillary sinus) bacterial contamination of
the implant surface during placement, premature
loading leading to bone micro-fractures, poor bone
quality.
203

Deep peri-implantitis

Kalyvas et al.

Figure 5 The removed part of the implant and the periapical lesion.
Figure 7 Post-operative X-ray taken after a 7 years period of follow-up.

Figure 8 Panoramic X-ray after the implant placement.

Figure 6 The surgical eld after the apicoectomy of the implant.

As mentioned before, according to Sussman, when

an implant insertion results in devitalisation of a tooth
(e.g. due to insufficient distance, bone overheating and
cutting off the blood supply to the pulp), it can cause an
endodontic pathology that consequently may infect
the implant (pathway 1). A periapical lesion from a
nearby devitalised tooth (pathway 2) can encroach
upon the implant and contaminate it (e.g. reactivation
of a dormant periapical lesion or removal of the periapical endodontic seal). As far as the inactive lesion is
concerned, it is usually caused by placing implants that
are shorter than the drilled cavity or by a heat-induced
aseptic bone necrosis.
It was suggested that dental implants do not possess
the ability to withstand any bacterial challenge during
the first stage of osseointegration and that bacteria or
endotoxins can travel through marrow spaces and
contaminate an adjacent implant19. However, there is a
204

debate regarding if and when bacteria are present in

periradicular lesions. Even in the absence of viable
bacteria, surfaces from clinically ailing or failing
implants have been shown to be contaminated with
endotoxin, which apparently can prevent biologic
repair. Presumably, the presence of endotoxins could
induce deep peri-implantitis, when their origin is the
apex of the extracted tooth or the adjacent failed root
canal treatment19. On the other hand, Flanagan
believes that the bone at the implant site may contain
residual encapsulated bacteria, which are activated by
the implant osteotomy, reinstating the infection at the
apex of the implant4. Additionally, it is proposed that
apical entrapment of gingival epithelial cells during the
placement phase of treatment may be a cause of deep
peri-implantitis and that a small perforation of the cortical bone at the apical end of the osteotomy could
provide a path of least resistance for an infectious
process and a fistula formation4.
Oral Surgery 8 (2015) 200--207.
2014 The British Association of Oral Surgeons and John Wiley & Sons Ltd

Kalyvas et al.

Figure 9 Clinical aspect of the stula.

Deep peri-implantitis

Figure 11 The surgical eld after the apicoectomy of the implant.

Figure 12 Post-operative X-ray after a 10 years period.

Figure 10 Gutta-percha pointing the origin of the inammation. The relation with the adjacent non-healed extraction socket is a matter of radiographic projection.

It is noted that in both cases, the maxillary premolar

region is involved. This is consistent with the observations of Quirynen et al. (2005)14, as well as the data
presented in Table 1. Additionally, both the affected
implants were 15 mm long, which suggests that a possible cause of deep peri-implantitis in these cases was
bone overheating during implant placement. The bone
at the apical part of the prepared implant site may not
be adequately cooled with saline irrigation during
drilling when the site walls are as deep as 15 mm.
However, in the first case, there is no dental record for
the extracted tooth 15 and, therefore, the remaining
inflammatory cells or bacteria from a periapical lesion
cannot be excluded as a possible cause. As far as the
second case is concerned, the lesion can also be attribOral Surgery 8 (2015) 200--207.
2014 The British Association of Oral Surgeons and John Wiley & Sons Ltd

uted to the fact that the implant at site 14 was placed in

close proximity to the root of tooth 13 and its periapical
lesion.
In order to treat deep peri-implantitis, several
approaches have been proposed. They include surgical
debridement (curettage), implant detoxification,
guided tissue regeneration, apical resection and
implant removal (Table 2). There are no randomised
control trials available for none of the treatment
options. According to Oh et al., implant removal is the
preferable treatment for mobile implants6. Otherwise,
surgical intervention, that is, the removal of inflamed
granulation tissue, is indicated. Detoxification is the
disinfection of the implant surface by chemical means,
such as citric acid, chlorhexidine gel, tetracycline
and/or hydrogen peroxide13. However, because of the
rough surfaces on some implants, the mechanical
management of contaminated implant surfaces is difficult. In addition, Shabahang et al. report that the results
205

Deep peri-implantitis

Kalyvas et al.

Table 2 Treatment of deep peri-implantitis

Authors
Ayangco and Sheridan

Chaffee et al.22
Brisman et al.23

Flanagan4
Oh et al.6
Quirynen et al.24

Tseng et al.12
Bousdras et al.25
Tzm et al.8
Kalyvas et al. (2009)
Mohamed et al.18

13

Treatment

Follow-up

a. Antibiotics, debridement, detoxication with tetracycline paste

b. Debridement, detoxication with tetracycline paste, amoxicillin 500 mg 3 7
c. Debridement, detoxication with tetracycline paste
Debridement, Guided Bone Regeneration, amoxicillin 500 mg 3 10, endodontic treatment of
45, 14 months later retreatment of 45
a. Implant removal
b. Implant removal
c. Implant removal
d. Drainage, clindamycin 300 mg 4 2 and 150 mg 4 7, surgical debridement
Penicillin 500 mg 4 7 and hydrocodone, debridement, placement of calcium hydroxide paste
Implant removal, apicoectomy of adjacent tooth, new implant 3 months later
a. Doxycycline 100 mg 10, debridement
b. Antibiotics, debridement, GBR
c. Implant removal
d. Implant removal
Implant removal, GBR, new implant 4 months later
Metronidazole 400 mg 3 7, debridement and apicoectomy, chlorhexidine mouthwash
Endodontic treatment of 11, surgical debridement, apicoectomy of 11, GBR, amoxicillin
500 mg 4 10, chlorhexidine mouthwash
a. Amoxicillin 500 mg 3 8, apicoectomy and tissue regeneration
b. Amoxicillin 500 mg 3 8, apicoectomy and tissue regeneration
a. Debridement and detoxication
b. Xenograft and platelet-rich brin

a. 8 months
b. 1 year
c. 8 years
18 months

of their experimental study indicated that detoxification of the implant surface did not have a positive
impact on the amount of osseointegration19. Therefore,
implant apicoectomy appears to be an effective treatment method. Balshi et al.5 report that 38 of 39 (97.4%)
resected implants remained stable and functional. The
follow-up time averaged 4.54 years, whereas the
longest exceeded 15 years.

Conclusion

3.

4.

5.

In conclusion, as both cases have a long follow-up

period (7 and 10 years), the implant apicoectomy can
be considered as a safe and reliable treatment with
long-term success.

6.

Conflict of interest

7.

The authors confirm that they have no conflict of

interest.
8.

References
1. Sussman HI, Moss SS. Localized osteomyelitis secondary to endodontic-implant pathosis. A case report.
J Periodontol 1993;64:30610.
2. Laird BS, Hermsen MS, Gound TG, Al Salleeh F,
Byarlay MR, Vogt M et al. Incidence of endodontic
implantitis and implant endodontitis occurring with
206

9.

11 months
a. 1 year
b. 3 years

Regular recall
2 years
6 months
a.
b.
a.
b.

7 years
10 years
4 months (loading)
1 year

single-tooth implants: a retrospective study. J Endod

2008;34(11):131624.
Dahlin C, Nikfarid H, Alsen B, Kashani H. Apical periimplantitis: possible predisposing factors, case reports
and surgical treatment suggestions. Clin Implant Dent
Relat Res 2009;11(3):2227.
Flanagan D. Apical (retrograde) peri-implantitis: a case
report of an active lesion. J Oral Implantol
2002;28(2):926.
Balshi SF, Wolfinger GJ, Balshi TJ. A retrospective
evaluation of a treatment protocol for dental implant
periapical lesions: long-term results of 39 implant
apicoectomies. Int J Oral Maxillofac Implants
2007;22:26772.
Oh T, Yoon J, Wang H. Management of the implant
periapical lesion: a case report. Implant Dent
2003;12:416.
Reiser GM, Nevins M. The implant periapical lesion:
etiology, prevention, and treatment. Compend Contin
Educ Dent 1995;16:768, 770, 772 passim.
Tzm TF, Senimen M, Ortakoglu K, zdemir A,
Aydin C, Keles M. Diagnosis and treatment of a large
periapical implant lesion associated with adjacent
natural tooth: a case report. Oral Surg Oral Med Oral
Pathol Oral Radiol Endod 2006;101:1328.
Jalbout ZN, Tarnow DP. The implant periapical lesion:
four case reports and review of the literature. Pract
Proced Aesthet Dent 2001;13(2):10712.

Oral Surgery 8 (2015) 200--207.

2014 The British Association of Oral Surgeons and John Wiley & Sons Ltd

Kalyvas et al.

10. Penarrocha-Diago M, Boronat-Lopez A, Garcia-Mira B.

Inflammatory implant periapical lesion: etiology, diagnosis, treatment presentation of 7 cases. J Oral
Maxillofac Surg 2009;67(1):16873.
11. Scarano A, Di Domizio P, Petrone G, Iezzi G, Piatelli A.
Implant periapical lesion: a clinical and histologic
report. J Oral Implantol 2000;26:10913.
12. Tseng C, Chen YM, Pang I, Weber H. Peri-implant
pathology caused by periapical lesion of an adjacent
natural tooth: a case report. Int J Oral Maxillofac
Implants 2005;20:6325.
13. Ayangco L, Sheridan PJ. Development and treatment
of retrograde periimplantitis involving a site with a
history of failed endodontic and apicoectomy procedures. Int J Oral Maxillofac Implants 2001;16:412
17.
14. Quirynen M, Vogels R, Alsaadi G, Naert I, Jacobs R, van
Steenberghe D. Predisposing conditions for retrograde
peri-implantitis, and treatment suggestions. Clin Oral
Implants Res 2005;16:599608.
15. Zhou W, Han C, Li D, Li Y, Song Y, Zhao Y. Endodontic
treatment of teeth induces retrograde periimplantitis.
Clin Oral Implants Res 2009;20(12):132632.
16. Bretz WA, Matuck AN, De Oliveira G, Moretti AJ, Bretz
WA. Treatment of retrograde peri-implantitis: clinical
report. Implant Dent 1997;6(4):28790.
17. Ataullah K, Chee LF, Peng LL, Lung KHH. Management
of retrograde periimplantitis: a clinical case report.
J Oral Implantol 2006;32(6):30812.

Oral Surgery 8 (2015) 200--207.

2014 The British Association of Oral Surgeons and John Wiley & Sons Ltd

Deep peri-implantitis

18. Mohamed JB, Alam NM, Singh G, Chandrasekaran SC.

The management of retrograde peri-implantitis: a case
report. J Clin Diagn Res 2012;6(9):16002.
19. Shabahang S, Bohsali K, Boyne PJ, Caplanis N, Lozada
J, Torabinejad M. Effect of teeth with periradicular
lesions on adjacent dental implants. Oral Surg Oral Med
Oral Pathol Oral Radiol Endod 2003;96:3216.
20. Steiner DR. The resolution of a periradicular lesion
involving an implant. J Endod 2008;34(3):3305.
21. McAllister BS, Masters D, Meffert RM. Treatment of
implants demonstrating periapical radiolucencies. Pract
Periodontics Aesthet Dent 1992;4:3741.
22. Chaffee NR, Lowden K, Tiffee JC, Cooper LF. Periapical
abscess formation and resolution adjacent to dental
implants: a clinical report. J Prosthet Dent 2001;85:
10912.
23. Brisman DL, Brisman AS, Moses MS. Case reports.
Implant failures associated with asymptomatic
endodontically treated teeth. J Am Dent Assoc
2001;132:1915.
24. Quirynen M, Gijbels F, Jacobs R. An infected jawbone
site compromising successful osseointegration. Periodontol 2000 2003;33:12944.
25. Bousdras V, Aghabeigi B, Hopper C, Sindet-Pedersen S.
Management of apical bone loss around a mandibular
implant: a case report. Int J Oral Maxillofac Implants
2006;21:43944.
26. Sussman HI. Periapical implant pathology. J Oral
Implantol 1998;24:1338.

207