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J Clin Periodontol 2014; 41: 779–790 doi: 10.1111/jcpe.

12265

Systematic Review
Treatment of periodontal- Julia C. Schmidt†, Clemens Walter†,
Mauro Amato and Roland Weiger

endodontic lesions – a
Department of Periodontology,
Endodontology and Cariology, University of
Basel, Basel, Switzerland

systematic review †
Both authors contributed equally to this work.

Schmidt JC, Walter C, Amato M, Weiger R. Treatment of periodontal-endodontic


lesions – a systematic review. J Clin Periodontol 2014; 41: 779–790. doi: 10.1111/
jcpe.12265.

Abstract
Background: The treatment of periodontal-endodontic lesions is challenging due
to the involvement of both periodontal and endodontic tissues.
Objective: To evaluate the treatment options and outcomes of periodontal-
endodontic lesions.
Material and Methods: A systematic literature search was performed for articles
published by 12 May 2013 using electronic databases and hand search. Two
reviewers conducted the study selection, data collection and validity assessment.
The PRISMA criteria were applied. From 1087 titles identified by the search
strategy, five studies and 18 case reports were included.
Results: Clinical studies and case reports were published from the years 1981 to
2012. A pronounced heterogeneity exists among studies regarding applied treat-
ment protocols and quality of reporting. In all clinical studies, comprising 111
teeth, a non-surgical root canal treatment (RCT) was performed as initial treat-
ment step. Non-surgical and/or a surgical periodontal therapy was applied in
some studies without re-evaluation of the endodontic healing. Probing pocket
depth reductions were reported in all included studies, comprising the data from
Key words: periodontal surgery;
80 teeth at follow-up. periodontitis; pulp necrosis; root canal
Conclusions: A sequential treatment with root canal treatment as a first treatment treatment
step appears to be reasonable. An adequate time for tissue healing is suggested
prior to re-evaluation. Accepted for publication 21 April 2014

A communication between the peri- e.g. so-called periodontal-endodontic e.g. altered response to pulp sensibi-
odontium and the dental pulp exists lesions. lity testing, multiple or singular incre-
through different pathways inclu- An endodontic lesion may elicit an ased periodontal probing depth, sinus
ding the apical foramina, lateral and inflammatory response in the adja- tract, pus, radiological J-shaped lesi-
accessory canals or exposed dentinal cent periodontal tissue and thus can on or infrabony defect (Harrington
tubules (Seltzer et al. 1963, Rotstein cause a retrograde periodontitis (Sim- 1979, Abbott 1998). The retrospective
& Simon 2006). These anatomical ring & Goldberg 1964). A periodontal identification of the primary cause
structures enable the development lesion may provoke an extensive pulp of a periodontal-endodontic lesion,
of diseases with concurrent periodon- pathosis (Langeland et al. 1974, however, is not possible in most
tal and pulpal tissue involvement, Bergenholtz & Lindhe 1978). In addi- cases.
tion, periodontal and endodontic di- Several classification systems
Conflict of interest and source of seases can develop independently. were applied to describe these
funding Teeth with a periodontal-endodontic lesions according to their pathogene-
lesion feature an inflamed or necrotic sis or with respect to a suggested
The authors declare that they have no pulp tissue and increased probing therapy sequence (Simon et al. 1972,
conflicts of interest. No external fund- pocket depths leading to great vari- Guldener 1975, Geurtsen et al. 1985,
ing was obtained for this review. ability of possible diagnostic findings, Dietrich et al. 2002). However, the
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 779
780 Schmidt et al.

classification is still under an ongo- dix S1). The research questions were Study selection
ing scientific debate (Simon et al. adapted using the PICO (Patient, The combinations of search terms
1972, Abbott & Salgado 2009). The Intervention, Comparison, Outcomes) resulted in a list of 1087 titles from
current classification of periodontal criteria (Miller & Forrest 2001). the electronic databases (Fig. 1).
diseases, even controversely discus- Two of the authors (M. A. and J.
sed, postulates the category “combi- S.) screened the titles and abstracts
Eligibility and ineligibility criteria
ned periodontal-endodontic lesion” for compliance with the inclusion
irrespective of the suspected patho- Publications were considered eligible criteria and selected 186 publications
genesis of the lesion (Armitage 1999, for inclusion in this systematic for full text analysis. A third
Lang et al. 1999, Eickholz 2013). review if they presented the follow- reviewer (C. W.) reassessed both the
The treatment of these lesions is ing parameters: (1) the presence of a included and excluded studies.
a challenge and treatment planning combined periodontal-endodontic
needs to consider the involvement of lesion defined as the co-existence of
Data collection process
the periodontal and pulpal compart- a negative or altered pulp vitality
ment. A wide spectrum of different test and PPD ≥6 mm on at least one Data items
therapeutic options and/or therapeu- tooth site in case reports or a mean
The relevant data of included publi-
tic sequences including endodontic probing pocket depth ≥6 mm in
cations were collected in data extrac-
and periodontal treatment with non- interventional studies and case series
tion files.
surgical and/or surgical procedures and (2) a follow-up after treatment
with or without local or systemic of at least 6 months. No restrictions Risk of bias in individual studies
antibiotics has been described in case in terms of type of publication, i.e.
reports and clinical studies. case report, clinical study, review, The included studies were evaluated
language and time point of publica- by modified items from the Cochrane
tion were applied. Review articles Collaboration‘s Tool for assessing
Review of Current Literature risk of bias (Graziani et al. 2012)
were screened for the presentation of
case reports within the review. A (Appendix S3). Considering the ade-
Objective quacy in the respective studies, the
publication considered ineligible for
The purposes of the present syste- inclusion was hierarchically catego- items were graded and the percent-
matic review were to identify the rized (Appendix S4 and S5). age of positively graded items was
treatment options and to evaluate calculated (Graziani et al. 2012).
the therapy with respect to the out- Summary measures
Outcome measures
comes of combined periodontal-end-
odontic lesions in humans with The primary outcome measure was Most studies reported on mean PPD
respect to tooth loss and probing tooth loss after treatment of com- with standard deviations at baseline
pocket depth (PPD) reduction. bined periodontal-endodontic lesions. and at follow-up, but also individual
Changes in PPD, probing attachment values or the range of individual val-
level (PAL), gingival recession (REC) ues were presented.
The specific questions addressed in this
systematic review were: and radiographic findings were eval- Synthesis of results
uated as secondary outcome vari-
In patients with combined periodon- ables. Owing to the limited number of ran-
tal-endodontic lesions: domized controlled clinical trials and
• Which treatments/treatment
Information sources
the significant heterogeneity in
sequences were applied? reported treatment protocols, a pool-
• In case the treatment was per- The electronic databases MEDLINE ing of data or statistical meta-
formed at different time points, by OVID and EMBASE and the analyses were not appropriate and
what was the time interval for grey literature (www.opengrey.eu) therefore not performed.
re-evaluation of the first treat- were searched for studies published
ment step? prior to May 12, 2013. A hand
Results
• Which rates of tooth loss occurred search was performed on Journal of
after treatment? Clinical Periodontology, Journal of

Study selection
Does treatment of combined peri- Periodontology, Journal of Endodon-
odontal-endodontic lesions lead tics and International Endodontic A total of 1087 titles from the elec-
to a PPD reduction? Journal from January 1990 to May tronic databases were identified
2013. Moreover, the references of (Fig. 1). The titles and abstracts
publications examined for inclusion were screened by two reviewers (ob-
Material and Methods
were thoroughly analysed to search served agreement = 90.16%, kappa =
for additional publications. 0.773). The full texts of 186 publica-
Protocols
tions (selected by at least one
The present systematic review consi- reviewer) were further analysed. Full
Literature search
ders the PRISMA (Preferred Repor- text analysis led to exclusion of
ting Items for Systematic Review The search protocols in the different further 171 studies (Appendix S4
and Meta-analyses) criteria (Liberati databases were validated and created and S5). Finally, 15 publications from
et al. 2009, Moher et al. 2009) (Appen- as identical as possible (Appendix S2). the electronic search satisfied the
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Treatment of perio-endo lesions 781

analysed in 111 teeth. Most publica-


tions examined various tooth types
including both single- and multi-
rooted teeth (Ratka-Kr€ uger et al.
2000, Sun & Liu 2009, Li et al.
2012). A total of 68 molars, 22
bicuspids, 20 incisors and one unspe-
cified tooth were analysed. Two case
series stated the proportion of upper
and lower teeth with a large majority
of teeth in the mandibula (Haueisen
et al. 2000, Ratka-Kr€uger et al. 2000).
The mean PPD at baseline ranged
from 6.01  0.31 mm to 14.29 
1.76 mm (Hassan et al. 1986, Li et al.
2012). The individual PPD values
ranged from 9 to 17 mm (Hassan
et al. 1986, Haueisen et al. 2000).
Clinical symptoms in terms of pain,
thermal sensitivity, gingival swelling,
pus discharge from gingival margin,
increased mobility and sensitivity to
percussion were occasionally reported
(Haueisen et al. 2000, Ratka-Kr€ uger
et al. 2000, Sun & Liu 2009, Li et al.
2012). The appearance of a sinus tract
was reported in some patients
(Haueisen et al. 2000, Ratka-Kr€ uger
et al. 2000). In two case series, all
included teeth demonstrated either a
caries profunda treatment combined
with a filling or a crown restoration
(Haueisen et al. 2000, Ratka-Kr€ uger
et al. 2000). The presence of a
restoration or a carious lesion was
not reported in the remaining
publications.
Fig. 1. Selection process of the studies included (Moher et al. 2009).
The radiographic findings were
described as periapical, lateral and/or
inclusion criteria. Eight additional Li et al. 2012). The patients‘ age in inter-radicular radiolucencies (Hauei-
publications were identified by screen- two other publications ranged from sen et al. 2000, Ratka-Kr€ uger et al.
ing the references of studies evaluated 25 to 53 years (Hassan et al. 1986, 2000, Li et al. 2012). Moreover,
for inclusion. Sun & Liu 2009), whereas it was not Ratka-Kr€ uger et al. (2000) specified
available in one case series (Ratka- the pattern of bone loss on radio-
Description of characteristics, results, and
Kr€uger et al. 2000). The proportion graphs as local and narrow, extending
quality assessment of females and males was provided to the apex and frequently without
in two publications including each any approximal bone loss.
The analysis for clinical studies and 18 males and 12 females (Sun & Liu
case reports was performed sepa- In patients with combined periodon-
2009, Li et al. 2012). Two studies
rately. The characteristics of included tal-endodontic lesions:
stated exclusion criteria in terms of
studies (Table 1) and case reports the presence of systemic diseases, Which treatments/treatment sequences
(Table 2, Appendix S6) and the asses- increased mobility of teeth, tobacco were applied? Different treatments of
sment of risk of bias (Appendix S7) use, pregnancy and the use of antibi- combined periodontal-endodontic
are summarized in tables. otics during the observation period lesions, including periodontal and
(Hassan et al. 1986, Li et al. 2012). endodontic approaches with non-
Summary of characteristics (PICO –
Three case series did not assign any surgical and surgical methods were
Population, Intervention/Comparison,
exclusion criteria (Haueisen et al. performed. In all publications, a non-
Outcomes)
2000, Ratka-Kr€ uger et al. 2000, Sun surgical root canal treatment was
Population – number and characteris- & Liu 2009). performed as initial treatment step.
tics of patients and tooth sites. The The included publications investi- A two-staged RCT with a temporary
mean age of patients in two of the gated each between 10 and 37 teeth. intracanal medication was applied in
included publications amounted 44 Overall, the treatment of combined two case series. After re-evaluation
and 51.2 years (Haueisen et al. 2000, periodontal-endodontic lesions was no further endodontic or periodontal
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
782

Table 1. Characteristics of included studies


First Study design Number of Tooth type Clinical Radiographic Additional Treatment Follow-up † Calculated PPD at follow-up Additional outcomes Number Confounding
author teeth and (n) manifestations manifestations diagnosis sequence tooth loss of factors
(year of patients, age, (n) (n) (n) (n) drop-outs considered
publication) gender, (patients)
Schmidt et al.

exclusion and
criteria reasons

Hassan Prospective 14 teeth Maxillary  Mean PPD – – SRP + Occl – (2 w) – +6 mo 2 6.125  4.076 mm Mean attachment 2, NFD Tooth type,
et al. case series 14 patients and 14.29  RCT1 (GP, (mean  SD) gain age,
(1986) 25–40 yrs mandibular 1.76 mm (range LC) + PS (RBF, In 10 patients: 3.2– 8.16  2.9 mm systemic
Exclusion incisors (14) 12–17 mm) D) + root 5.2 mm (range) In 10 patients: diseases
criteria:  No vitality demineralization In 2 patients: 14.2 mm attachment gain
systemic (citric acid) –15.3 mm (range) 7.9–11 mm
(14)
diseases, in 2 patients:
teeth attachment gain
excessively 2.8 mm–1.7 mm
mobile/ Radiographic signs of
requiring partially bone fill,
splinting continuity of
lamina dura
Haueisen Retrospective 10 teeth Mandibular  Narrow PPD Periradicular (mesial Fistula (4) RCT1 – (CD, 3 w) – +6 mo 0 2–4 mm (range) No inflammation, no 0 Tooth type,
et al. case series 51.2 yrs molars (10) 9–12 mm (10) and/or distal) and RCT2 (GP, S, LC) FI, no increased age
(2000) (mean)  Pain (1) interradicular mobility, no

 Pus discharge radiolucency (10) sensitivity to

from gingival percussion,


radiographic signs
margin (3)
of complete bone
 FI (7)
repair (2) or
 Mobility grade I
advanced bone
(2), grade II (2)
repair (8)
 No vitality (7),
+ 12 mo 0 2–4 mm (range) Radiographic signs of 0
unclear response
complete bone
to pulp test (3) repair (except two
 Sensitivity to second molars with
percussion (2) horizontal bone
 Cp treatment loss of 1–2 mm)
and filling (2),
crown or partial
crown (8)

© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Table 1. (continued)
First Study design Number of Tooth type Clinical Radiographic Additional Treatment Follow-up † Calculated PPD at follow-up Additional outcomes Number Confounding
author teeth and (n) manifestations manifestations diagnosis sequence tooth loss of factors
(year of patients, age, (n) (n) (n) (n) drop-outs considered
publication) gender, (patients)
exclusion and
criteria reasons

Ratka-Kr€
uger Retrospective 20 teeth Mandibular  Mean PPD Local narrow bone Fistula RCT1 – (CD, within +6 mo 5 3.1 mm (mean) No FI in 10 of 15 5, NFD Tooth type
et al. case series molars (15), 11.3 mm loss to apex, 2 mo) – RCT2 molars,
(2000) maxillary  Swelling and/or interradicular and/ (GP, S, LC) radiographic signs
molars (4), pus discharge or periapical of improvement up
other from gingival radiolucency to complete
tooth (1) without regeneration in
margin
interproximal bone most teeth
 FI (18)
loss in molars, +12 mo 11 2.2 mm (mean) No FI in 6 of 9 11, NFD
 No vitality or
periapical molars,
unclear response
radiolucency (>0.5 radiographic signs
to pulp test (20)
of root length) with of improvement up
 Sensitivity to per-
widened to complete
cussion some- periodontal regeneration in
times unclear ligament space most teeth
 Cp treatment
and filling (9),
crown or partial

© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
crown (11)

Sun & Liu Prospective 37 teeth Bicuspids Teeth with 6 mo Bone loss – RCT1 – (1 w) – +6 mo 8 2.83  0.149 mm* Mean CAL 8, NFD Tooth type,
(2009) case series 30 patients (13), molars follow-up (n = 29) Occl + SRP – (4 w) 6.79  0.182 mm* age,
28–53 yrs (24)  Mean PPD – PS (MWF, BGa, Mean mobility experience of
18 male, 6.62  0.230 mm D, AB amox/ 1.38  0.092* therapist
12 female Mean CAL metro) +12 mo 18 2.42  0.233 mm* Mean CAL 18, NFD

8.76  0.209 mm 6.58  0.268 mm*
Mean mobility
 Mean mobility
1.26  0.104*
1.66  0. 134
Teeth with 12 mo
follow-up (n = 19)
 Mean PPD
6.74  0.285 mm
 Mean CAL
8.79  0.282 mm
 Mean mobility
1.68  0.172
 Pain
 Swelling
 No vitality (37)
Treatment of perio-endo lesions
783
Table 1. (continued)
784

First Study design Number of Tooth type Clinical Radiographic Additional Treatment Follow-up † Calculated PPD at follow-up Additional outcomes Number Confounding
author teeth and (n) manifestations manifestations diagnosis sequence tooth loss of factors
(year of patients, age, (n) (n) (n) (n) drop-outs considered
publication) gender, (patients)
exclusion and
criteria reasons

Li et al. Prospective 30 teeth Test: Control: Periapical, lateral – Control: +3 mo 0 Control: Control: 0 Tooth type,
Schmidt et al.

(2012) randomized 30 patients anterior  Mean PPD and/or RCT1 (RF, S,  5.43  0.26 mm  Mean CAL age,
controlled 44 yrs (mean) teeth (2), 6.04  0.37 mm interradicular LC) + SRP (mean  SD) 1.15  0.21 - smoking,
trial 18 male, bicuspids (5),  Mean CAL radiolucency Test: Test: mm systemic
12 female molars (8) 1.60  0.19 mm Control: RCT1 (RF, diode  4.77  0.25 m- Mean mBI diseases,

Exclusion criteria: Control: anterior  Mean mBI 1.86  Mean PAI laser irradiationb, m** 0.80 experience
systemic teeth (4), 3.27 S, LC) + SRP of therapist
Test: (mean  SD) Test:
diseases, bicuspids (4), Test: (diode laser
 Mean PPD  Mean CAL
c
smoking, molars (7)  Mean PAI irradiation )
6.01  0.31 mm 1.06  0.19 -
pregnancy, 3.20
 Mean CAL mm
antibiotic intake
1.57  0.20 mm  Mean mBI
during
0.67
observation  Mean mBI 1.93
period
 Increased mobil-
ity

 No vitality (30) +6 mo 0 Control: Control: 0

 5.64  0.33 mm  Mean CAL


(mean  SD) 1.01  0.14 -
Test: mm
 4.34  0.23 m-  Mean mBI
m** (mean  0.60
SD)  Mean PAI
3.00
Test:
 Mean CAL
0.67  0.12 -
mm**
 Mean mBI
0.13**
 Mean PAI
2.47

a
xenograft; b1,5 W, continuous wave, one application (15 s); c1 W, continuous wave, one application daily (15 s) for 5 days; AB, systemic antibiotics; amox, amoxicillin; BG, bone graft;
CAL, clinical attachment loss; CD, calcium hydroxide dressing; Cp, caries profunda; D, periodontal dressing; FI, furcation involvement; GP, gutta percha; LC, lateral condensation; M,
membrane; mBI, modified bleeding index; metro, metronidazole; mo, months; MWF, modified Widman flap; NFD, not further described; Occl, occlusal adjustment; PAI, periapical index;
PPD, probing pocket depth; PS, periodontal surgery; RCT, root canal treatment; RBF, reverse bevel flap; RF, rotary files; S, sealer; SRP, scaling and root planing; w, weeks; yrs, years.
*p < 0.05 (difference between baseline and outcome).
**p < 0.05 (difference between control and test group); the wording used in the table was adapted from the publications included.

Time related to last treatment step.

© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Table 2. Characteristics of included case reports
First author Gender Age Perio* Smoking Tooth PPD (mm) Clinical Radiographic Additional Treatment sequence Follow-up PPD (mm) Additional
(year of type at manifestations manifestations diagnosis (mo)‡ at outcomes
publication) baseline† follow-up–

Moucachen M 50 NR NR 38 12 NV, Per A, L – Extraction – – –


et al. (1981)
Geurtsen et al. F 17 NR NR 46 13 NV, R A, L, IR, – Extraction – – –
(1985) wPLS
Stamas & M 64 NR NR 26 7 NV, Pu, M0, A, L, IR – RCT1 + RCT2 12 2–3 BF
Johnson R
(1994)
Haueisen et al. M 59 NR NR 36 12 UV, Pu, Per, A, L – RCT1 + RCT2 18 2 BF
(1999) R
Haueisen et al. M 56 NR NR 46 12 UV, Pu, Per, A, L, IR – RCT1 + RCT2 12 2–3 BF
(1999) R
Ratka-Kr€ uger M 56 NR NR 47 12 NV, Pu, S, R, A, L, IR Ab, Fis RCT1 + RCT2 6 3 BF
et al. (1999) FI
Wood et al. M 62 NR NR 46 11 NV, Pa, Per, A, L, IR – RCT1 + RCT2 + SRP 6 3 No FI
(2003) C, R, FI
Zubery & F 23 AgP NR 22 10 NV, Pa, S, M2 A, L Ab RCT1 + SRP 21 2 BF, M0-1
Machtei (3 months) SRP
(1993)
Zucchelli F 39 P NR 12 12 UV, M3, Rec, A, L Fis RCT1 + SRP + Spl 36 3 BF, M0
(2007) infraBDh (4 months) PS (EMD,

© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
BGa, ABf)
Zehnder (2001) M 28 AgP NR 15 8 NV, Pu, Pa, L Fis RCT1 + SRP + RCT2 + 6 5 BF, M1,
Per, M3 RCT3 (4 months) AttG
PS 3 mm
Kresic (1994) M 70 NR NR 43 11 NV, R A, L – RCT1 + SRP 22 4 BF, nPLS
(6 months) PS
Zubery & F 23 AgP NR 11 10 NV, Pa, S, A, L Fis RCT1 + SRP 12 2 BF, M0-1
Machtei M2, bBLh (3 months) SRP -
(1993) (9 months) – PS + ES
Walter et al. M 53 ChP HS 32 8i NV, R, Feh, A, L – RCT1 + RCT2 18 4 BF
(2008) infraBDh (14 months) PS
(BGa, Mb, ABf)
Danesh-Meyer M 40 NR NR 36 12 NV, Pu, R, L – RCT1 + PS (BGc, 6 2 BF, AttG
(1999) FIh, infraBDh Md, ABf) + RCT2– 8 mm
(4 months) RCT3
Haueisen & F 62 NR NR 46 12 NV, Pu, Pa, A, L, IR – RCT1 + PS (Res) + Spl 12 1 BF, M1
Heidemann Per, S, M2,
(2002) R, FIh
John et al. F 58 NR NR 21 14 NV, M2, L – RCT1 + Spl + PS 9 4 BF, M1
(2004) infraBDh (EMD, BGa, ABf)
Yavuz et al. M 25 NR NR 22 7 NV, S, bBLh, A, L, AccR Fis RCT1 + RCT2 + PS 12 3–4 BF
(2008) infraBDh (Res, BGe, ABf)
Treatment of perio-endo lesions

Ghezzi et al. M 38 NR NR 21 9 NV, Pu, L – RCT1 + SRP + PS 24 3 BF


(2012) infraBDh, (BGa,e, Mb, ABf)
bBLh
785
786 Schmidt et al.

therapy was deemed to be necessary

HS, heavy smoker; infraBD, infrabony defect; IR, interradicular radiolucency; L, lateral radiolucency; M, male; Me, membrane; M, mobility (grade 0–3); nPLS, normal periodontal ligament
BOP, bleeding on probing; C, caries; ChP, chronic periodontitis; EMD, enamel matrix derivates; ES, endodontic surgery; F, female; Fe, fenestration; Fis, fistula; FI, furcation involvement;

space; NR, not reported; NS, non-smoker; NV, negative vitality test response; P, periodontitis (not further specified); Pa, pain; Per, positive percussion test; PS, periodontal surgery; Pu, pus;
xenograft; bbioabsorbable; calloplast; dnon-resorbable; eautograft; fsystemic application; glocal application; hintra-operative finding; idata from patients record; jallograft; A, apical radiolu-
cency; Ab, abscess; AB, antibiotics; AccR, accessory root; AgP, aggressive periodontitis; AttG, attachment gain; bBL, buccal bone loss; BF, radiographic signs of bone fill; BG, bone graft;

R, restoration; RCT, root canal treatment; Rec, recession; Res, root resection; S, swelling; Spl, splint; SRP, scaling and root planing; UV, unclear or delayed vitality test response; wPLS,
Additional
outcomes

BF, M0
BF, no
in these case series (Haueisen et al.

BOP

widened periodontal ligament space; + time between various treatment steps <3 months; for more details see Appendix S6. –PPD corresponding to the highest reported PPD at baseline.
2000, Ratka-Kr€ uger et al. 2000). The
remaining publications combined an
endodontic with a periodontal treat-
PPD (mm)

follow-up–
ment. Li et al. (2012) selected a non-
at surgical approach by combining a

2
root canal treatment with the root
debridement of involved teeth with
(test group) or without (control
Follow-up

group) diode laser irradiation. The


(mo)‡

10

12
laser was applied both during RCT
and after initial periodontal treat-
ment in a mode aiming in bacterial
reduction. Two publications added
Treatment sequence

periodontal surgery to a conven-


(12 months) PS
RCT1 + SRP + PS

tional non-surgical periodontal and


(BGe, Md, ABf,g)

(BGj, Mb, ABf,g)

endodontic treatment. Hassan et al.


(BGc) + ES

(1986) applied citric acid as condi-


RCT1 + PS

tioning agent to the root surfaces


within an open flap debridement.
Sun & Liu (2009) used a xenogenous
bone graft material and adjuvant
Additional

systemic antibiotics in addition to


diagnosis

surgery.

In case the treatment was performed


at different time points, what was the
manifestations
Radiographic

time interval for re-evaluation of the


first treatment step? In two retro-
spective case series non-surgical
A, L

endodontic treatment was performed


A

as a first treatment step and the deci-


manifestations

sion for any further therapy was left


NV, M2, R,

open and performed 6 months after


Clinical

Rec, FIh,
infraBDh

NV, M2

re-evaluation of the healing after


RCT (Haueisen et al. 2000, Ratka-
For calculation purposes, only the highest and clearly defined PPD was taken.

Kr€ uger et al. 2000). In both case


series, in all re-evaluated patients, no
PPD (mm)

baseline†

further therapy was deemed neces-


10
at

sary since the initial RCT was classi-


9

fied as successful according to


clinical and radiographic criteria. In
Tooth

the remaining publications, a com-


type

16

12

bined treatment was initially planned


using a research plan and applied
Gender Age Perio* Smoking

without further decision making


NR
NS

within the healing process.

Which rates of tooth loss occurred


NR

NR

after treatment? No tooth loss was


Time related to last treatment step.

reported in either publications. The


*General periodontal conditions.

reported drop-out rate was two out


50

19

of 14 (Hassan et al. 1986), 11 out of


20 (Ratka-Kr€ uger et al. 2000) and
18 out of 37 (Sun & Liu 2009). No
F

F
Table 2. (continued)

drop-outs were reported in the


remaining two publications. As rea-
Oh et al. (2009)

sons were not provided, patients


First author

Politis et al.
publication)

who dropped out were assumed to


may have lost their treated teeth and
(year of

(1986)

considered as “worst case” for the


calculation of tooth loss (Spriet &
a


© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Treatment of perio-endo lesions 787

Dupin-Spriet 1993, Myers 2000). Of and two retrospective case series, and treatment options and/or materials
the 111 treated teeth for 80 teeth an 18 case reports were included from a have changed dramatically over time
outcome was reported, leading to systematic literature search. Due to (Hassan et al. 1986, Li et al. 2012,
the assumption of 31 teeth may have an assumed scarcity of clinical studies, Rodriguez et al. 2013), probably
been lost during follow-up, repre- the initial purpose of this systematic leading to difficulties in comparison
senting a tooth loss rate within the review was to evaluate case reports among the studies.
range of 0 to 27.9%. supposed to be the best external evi- Although the English language is
dence on this subject. As intervention- commonly accepted as the language
Does treatment of combined periodon- al studies and case series, however, of scientific research, relevant exter-
tal-endodontic lesions lead to a PPD were also found fulfilling the inclusion nal evidence could also arise from
reduction? Probing pocket depth criteria (Fig. 1), the data were pre- studies in languages other than Eng-
reductions in terms of a decreased sented separately for clinical studies lish (Morrison et al. 2012), in parti-
mean PPD or a smaller PPD range (Table 1) and case reports (Table 2, cular from members of the BRIC
occurred from baseline to follow-up Appendix S6) according to the sus- countries (Brazil, Russia, India,
in all included publications for the pected hierarchy of best available China) or findings from the early
teeth at follow-up. Data are reported external evidence. days of scientific periodontology
after 6 months in all included publi- A plethora of classifications for (Schmidt et al. 2013). In addition, it
cations. Three case series provided lesions with periodontal and end- was suggested that positive research
additional data after 12 months odontic tissue involvement has been findings are more likely to be pub-
(Haueisen et al. 2000, Ratka-Kr€ uger proposed. Several authors suggested lished in an international English-lan-
et al. 2000, Sun & Liu 2009). the differentiation between the pri- guage journal whereas negative
mary cause(s) of the lesion, i.e. of results may be rather reported in a
The PPD after a follow-up of
periodontal or endodontic origin non English-language journal (Egger
6 months decreased from a mean
(Simon et al. 1972, Guldener 1975, et al. 2003). The influence of lan-
PPD of 14.29  1.76 to 6.125 
Geurtsen et al. 1985). However, the guage restrictions on the outcome of
4.076 mm (Hassan et al. 1986). The
correct identification of the disease systematic reviews is uncertain in
individual values of the PPD ranged
onset is frequently impeded and particular fields of medicine (Morri-
from 3.2 mm to 15.3 mm (Hassan
remains of speculative nature in son et al. 2012). The exclusion of non
et al. 1986).
many cases, due to an incomplete English-language studies from a sys-
In a randomized controlled trial,
dental history or critical results of a tematic review, however, may lead to
Li et al. (2012) reported a signifi-
pulp sensibility test, in particular in a language bias. The literature search
cantly different PPD reduction after
multi-rooted teeth. According to of the present systematic review was
a follow-up of 6 months from a
recent suggestions (Armitage 1999, performed without any language
mean PPD of 6.04  0.37 to 5.64 
Lang et al. 1999, Abbott & Salgado restrictions. Two original studies in
0.33 mm in the control group and
2009), in this systematic review, only Chinese language have been trans-
from a mean PPD of 6.01  0.31 to
publications that described a well lated. They fulfilled the inclusion cri-
4.34  0.23 mm in the test group.
defined feature of periodontal- teria and were included comprising
The PPD decreased from a
endodontic lesions, i.e. teeth with a 67 teeth out of 111 analysed teeth
mean PPD of 11.3 mm to 3.1 mm
negative or an unclear response to a (Sun & Liu 2009, Li et al. 2012).
after 6 months and to 2.2 mm after
pulp sensibility test and an increased Treatment planning includes the
12 months (Ratka-Kr€ uger et al.
probing pocket depth, were consid- consideration of diagnostic and prog-
2000). After a follow-up of 6 months,
ered (Appendix S4 and S5). Interest- nostic factors deemed to influence
the reported PPD range of 9 to
ingly, three studies included neither the treatment outcome of periodon-
12 mm at baseline declined to 2 to
used a classification system nor tal-endodontic lesions (Lang & To-
4 mm with no further changes up to
determined the disease onset proba- netti 2003, Kwok & Caton 2007).
12 months (Haueisen et al. 2000).
bly reflecting the difficulties and limi- However, in addition to mode of
A statistically significant reduc-
tations in differential diagnosis endodontic and/or periodontal treat-
tion of the PPD after 6 months, i.e.
(Hassan et al. 1986, Sun & Liu 2009, ment, potential confounding factors,
from a mean PPD 6.62  0.230 to
Li et al. 2012). e.g. patient‘s age, gender, tooth type,
2.83  0.149 mm and after 12 months,
The publications in this syste- smoking, periodontal history and
i.e. from mean PPD of 6.74  0.285
matic review were published within a chronicity of lesions, were inconsis-
to 2.42  0.233 mm was noted by
time frame from 1981 to 2012. As tently considered in the included
Sun & Liu (2009).
one finding from this review, non- publications resulting in a high risk
surgical RCT as a sole treatment of bias (Appendix S7). Further
Discussion
approach was performed by some research analysing the impact of
early publications whereas guided these factors on the pathogenesis and
Herein, we conducted a systematic tissue regeneration (GTR) proce- the outcome of therapy of periodon-
review to evaluate the best available dures were more frequently applied tal-endodontic lesions is required.
external evidence regarding the treat- in recent publications (Stamas & No tooth loss was reported except
ment options and outcomes of peri- Johnson 1994, Ghezzi et al. 2012). for two case reports. In case series
odontal-endodontic lesions. A total of Time point of publication needs to and case reports, success and/or sur-
five studies, i.e. one randomized con- be considered as a relevant parame- vival rates may be subject to a publi-
trolled clinical trial, two prospective ter within a review, because dental cation bias as a treatment success
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
788 Schmidt et al.

may be more likely to be published. 2008). In general, the evidence levels tors, e.g. a smoking habit (Walter
Therefore, treatment failures could refer to the study design suggesting et al. 2008, 2012b, Rodriguez et al.
be underrepresented. Several drop- randomized controlled clinical trials 2013). Similarly, the improvement of
outs occurred in three included publi- as higher available external evidence periodontal conditions subsequent to
cations (Hassan et al. 1986, Ratka- compared to other study designs scaling and root planing may take
Kr€uger et al. 2000, Sun & Liu 2009). (Hujoel 2008). For this reason, some several months, with the deeper the
Such drop-out rates pose a threat to authors feel there is a lack of direct initial PPD the longer the time for
validity of any study (Walter et al. evidence in case an (meta-analysis of) PPD reduction (Badersten et al.
2012a). In general, there are different RCT‘s is missing (Walter et al. 1984). An observation time of at least
possibilities to handle drop-outs 2012b, Schmidt et al. 2013, Walter & 6 to 12 months before re-evaluation
including the so-called “worst case” Friedmann 2013). In randomized of the first treatment step was sug-
analysis. As reasons for drop-outs controlled clinical trials, patients gested by Zehnder (Zehnder 2001).
were not provided, this method was need to be assigned to a predefined The publications included in this
applied in the present review and protocol. This design may exclude review reported a follow-up time
patients who dropped were assumed the opportunity of alteration of a between six and 12 months. However,
to may have lost their treated teeth treatment plan, which may be indi- with respect to the individual range of
(Myers 2000, Sutherland 2001, Wang cated after evaluation of the tissue the time required for periodontal tis-
et al. 2004). The tooth loss rate ran- response after root canal treatment. sue healing and the absence of radio-
ged from 0 to 27.9% resulting in a Healing of lesions of endodontic ori- graphic changes in early stages of
survival rate of 72.1 to 100%. The gin depends on many modifying fac- healing, the interpretation of treat-
survival rate may be affected by the tors and may occur within a large ment results after six to 12 months
eligibility criteria, including the PPD time frame (European Society of seems to be associated with some bias
range, applied in the randomized Endodontology 2006, Ricucci et al. (Hirsch et al. 1989, Jansson et al.
controlled clinical trial and in the 2009, Walter et al. 2008). Prospective 1997, Kim et al. 2008). The results
case series. For example, the exclu- case series or cohort studies permit from included studies and case series
sion of hypermobile and multi-rooted modifications of the treatment plan may need to be regarded as short-
teeth seems to be of prognostic rele- and sequence with respect to indivi- term outcomes. Follow-up examina-
vance and may have implications on dual healing responses and findings tions after an observation period of
the treatment outcome (Hassan et al. at different time points. A (prospec- several years would be desirable
1986). The herein reported survival tive) case series seems to be more although challenging.
rate is within the previously noted reasonable to evaluate the treatment With respect to the uncertain
range of survival rates. Schacher of periodontal-endodontic lesions at treatment outcome of periodontal-
et al. found a survival rate of 61% the current stage of knowledge. Four endodontic lesions and the successful
after at least 5 years to retain teeth case series and 18 case reports were outcome of less invasive treatment
with treated periodontal-endodontic included in this review. In two case approaches (Stamas & Johnson
lesions (Schacher et al. 2007). In series and four case reports including 1994, Haueisen et al. 1999, 2000,
addition, a prospective clinical trial five teeth, a non-surgical endodontic Ratka-Kr€ uger et al. 1999, 2000), the
reported a favourable outcome of treatment was performed as initial concept of a sequential treatment
77.5% in apicomarginal defects treatment and the decision for fur- with re-evaluation at different treat-
including periodontal-endodontic ther procedures were based on the ment stages may also be supported
lesions (Kim et al. 2008). In contrast tissue response at re-evaluation (Sta- from an economic point of view.
to the reported tooth loss and/or sur- mas & Johnson 1994, Haueisen et al. Financial costs and time efforts
vival rate, the PPD reduction repre- 1999, 2000, Ratka-Kr€ uger et al. increase dramatically with more
sents an alternative study end point, 1999, 2000, Walter et al. 2008). The invasive treatment approaches (Wal-
possibly representing a success rate remaining publications predefined ter et al. 2012c). On the other hand
from a strictly periodontal point of the treatment sequence, i.e. a com- patient-centred outcomes, including
view. A PPD reduction was achieved bined treatment consisting of non- quality of life, treatment time and
in nearly all re-evaluated teeth, but surgical endodontic therapy with a costs, are of increasing importance
there may be remaining deep probing non-surgical and/or a surgical peri- within clinical trials to ensure an
depths (Hassan et al. 1986, Li et al. odontal therapy. Periodontal surgery appropriate allocation of resources
2012). However, the PPD of the consisted of an open flap debride- (Br€agger 2005, Walter et al. 2012c).
included teeth differed remarkably ment alone or in combination with
between the clinical studies (Hassan regenerative or resective procedures.
Conclusions and Clinical Relevance
et al. 1986, Li et al. 2012). Keeping Incomplete tissue healing after
in mind, that a narrow localized deep evaluation of the first treatment step Taken together, this review may pro-
PPD may represent a draining sinus may lead to the decision of further vide some evidence for root canal
tract of endodontic origin that healed procedures (Dietrich et al. 2003). treatment as a first treatment step
after root canal treatment (Weiger Healing of periapical lesions may take for the treatment of combined peri-
et al. 1995, Abbott & Salgado 2009). up to 4 years (European Society of odontal-endodontic lesions with
The data from clinical studies and Endodontology 2006) or longer (Ric- increased PPD and a negative
case reports were analysed separately ucci et al. 2009). This process may be response of pulp sensibility testing.
with respect to the suspected hierar- modified by several hereditary, envi- A reasonable time for healing of the
chy of external evidence (Hujoel ronmental and behavioural risk fac- endodontic lesion after root canal
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Treatment of perio-endo lesions 789

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Principal findings: In this systematic Practical implications: The findings


Clinical Relevance review, a successful outcome in from this systematic review may
Scientific rationale for the study: terms of probing pocket depth support an initial root canal treat-
Different therapeutic approaches reduction of exclusive non-surgical ment for the treatment of this kind
including endodontic and/or peri- endodontic therapy was identified of periodontal-endodontic lesions.
odontal procedures have been pro- for teeth with a negative response to A reasonable time in advance of
posed for the treatment of pulp sensibility testing combined consideration of further procedures
periodontal-endodontic lesions. with increased probing pocket depth. is suggested.

© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

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