Accepted Manuscript

Title: Treatment of enucleated odontogenic jaw cysts. a systematic review.

Author: Buchbender M., Neukam F.W., Lutz R., Schmitt C.

PII: S2212-4403(17)31247-6
DOI: https://doi.org/10.1016/j.oooo.2017.12.010
Reference: OOOO 1911

To appear in: Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology

Received date: 27-9-2017

Accepted date: 13-12-2017

Please cite this article as: Buchbender M., Neukam F.W., Lutz R., Schmitt C., Treatment of
enucleated odontogenic jaw cysts. a systematic review., Oral Surgery, Oral Medicine, Oral
Pathology and Oral Radiology (2017), https://doi.org/10.1016/j.oooo.2017.12.010.

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TITLE

Treatment of enucleated odontogenic jaw cysts. A systematic review.

Buchbender M1 DDS, Neukam FW MD,DDS,PhD, Professor and Chair 1, Lutz R MD,DDS1,

Schmitt C DDS,MSc,PhD1
1
Department of Oral and Maxillofacial Surgery, University of Erlangen- Nuremberg,

Erlangen, Germany

Corresponding Author

Dr. Mayte Buchbender

Department of Oral and Maxillofacial Surgery,

University of Erlangen- Nuremberg,

Glückstrasse 11,

91054 Erlangen, Germany

Phone: +49 9131 85 33614

Fax: +49 9131 85 33657

E-mail: mayte.buchbender@uk-erlangen.de

Disclosures

No conflict of interest.

Word Count

Abstract: 198

Manuscript: 3.149

Number of figures: 1 Number of tables: 2

Page 1 of 19
Statement of clinical relevance

The treatment of bone defects after enucleation of odontogenic jaw cysts for predictable bony
regeneration is not solid according to the current literature. The methodological approach to form
recommendations is heterogeneous. Therefore, comparative studies are needed.

Abstract

Objectives: In this systematic review, we aimed to assess the impact of filling or not filling

enucleated odontogenic jaw cysts on bony defect consolidation. In terms of filling we aimed

to assess which is the best filling material based on current evidence.

Study design: An electronic search was performed using PubMed, Embase, and Medline

databases with the logical operators: "odontogenic cysts” AND “jaw cysts" AND "treatment

AND therapy".

Results: Thirteen studies with primary enucleation (6 with filling and 7 without filling) were

included. In terms of filling either synthetic bone substitutes or autologous bone were used.

The primary outcome was bony regeneration judged by radiographic follow-up

measurements. 2D radiographic follow-up measurements (densitometry) revealed a bone

density increase and comparable bone regeneration in both groups.

Conclusions: Due to the low number of studies and the heterogeneity of the included data,

evidence based treatment recommendations cannot be given at this time. Also outcomes based

on 2D measurements should be interpreted with caution. However, the following factors are

suggested having an impact on bony defect consolidation: defect size, defect configuration,

the preservation of the periosteum and localization (upper or lower jaw). Prospective

comparable clinical studies with a 3D follow-up are needed.

Page 2 of 19
Introduction

Odontogenic jaw cysts can occur in every period of life. Their localisation (upper, lower jaw)
is very much dependent on the origin of the cyst. They can exist as single or multiple cavities
which are lined by a specific cyst epithelium. They are usually characterised by a small and
asymptomatic growth which mostly results in large bone cavities. The most occurring cysts
are radicular cysts followed by follicular cysts and keratocystic odontogenic tumors (KCOT)
1
. The new WHO classification of 2017 has reclassified the former KCOT as a cyst.
However, in this systematic review the term (KCOT) was used as it was defined in the
reviewed literature. The total removal of these cysts remains the primary aim to prevent their
recurrence. However, in the current literature, there is no clear recommendation for a specific
surgical approach. Basically two different operation techniques are described. The first is the
decompression technique 2-4 to create a communication of the cyst with the mouth and
therefore trigger appositional bone regeneration and reduce the diameter/volume of the cyst.
In this case mostly two surgical procedures are necessary to remove the cyst completely. This
technique should minimize patients’ morbidity and preserve sensitive structures (dependent
on localisation and size of the cyst). The other technique is the so called primary enucleation,
which means removing the cyst in total 5, 6. The resulting cavity can be left untreated, waiting
for spontaneous bone regeneration, either from the formed blood clot or the adjacent bone
walls covered by soft tissue 7-10. The other option is to fill the cavities with autologous bone or
bone substitute material 11. Different bone substitute materials are described as potential fillers
in these cases. However, literature lacks evidence to support one over the other treatment as
well as what kind of filling materials should be used. Moreover it is well documented in the
literature in animal studies, that bony defects larger than a so called critical size defect (CSD)
with <1cm3 do not show a hundred percent regeneration when left untreated 12.

The aim of this systematic review is to find evidence which supports filling defects after
enucleation or leaving them unfilled. In terms of the filling material, we also try to clarify
which is the perfect filler in terms of cavity regeneration.
3

Page 3 of 19
Material and Methods

This systematic review was conducted according to the Preferred Reporting Items for
Systematic Reviews and Meta- Analyses (PRISMA) statement, the recommendations of the
Cochrane Handbook for Systematic Reviews and known literature guidelines writing a
systematic review. Articles related to jaw lesions in the context with enucleation were
reviewed. The central review questions were as follows (“PICO” format; P= Patient/ problem/
population, I= Intervention, C= Comparison, O= Outcome):

1. In patients with odontogenic jaw cysts undergoing surgery (P) does filling vs. no
filling (I,C) show reliable osseous regeneration (O)?

2. In terms of filling, which bone substitute (I,C) leads to foreseeable defect regeneration
(O)?

Types of studies

Studies were included according to the following general inclusion criteria:

1. Publication in an international peer-reviewed journal;

2. Study published in English;

3. Publication not older than 15 years;

4. Only clinical studies dealing with at least 10 patients

5. Retrospective and prospective studies

Exclusion criteria:

1. Articles published in another language

2. Experimental or ex vivo studies

Page 4 of 19
3. Narrative or systematic reviews

4. Letters to the editor commentaries or abstracts

5. Case reports/ series

6. Studies regarding only KCOT’s

Publications not meeting all mentioned inclusion criteria, were excluded from this systematic
review. In the presence of duplicate publications, only the study with the most inclusive data
was selected.

Types of interventions

Only primary enucleation with or without cavity filling were included. Decompression alone
was excluded.

Types of outcome measures

Primary outcome

Bone regeneration (by means of radiographic follow-up measurements, 3- and 2D)

Secondary outcomes

1. Clinical outcome parameters

2. Surgical complications
3. Clinical or radiographic recurrence

Search Strategy

The following electronic databases were searched to identify relevant studies.

1. The Cochrane Library (up to November, 15th, 2016)

 The Cochrane Central Register of Controlled Trials (CENTRAL)
2. MEDLINE (up to November, 15th, 2016)
3. EMBASE (up to November, 15th, 2016)

Electronic search was carried out using the logical operators: (“odontogenic cysts AND jaw
cysts”) AND (“treatment AND therapy”). In addition a hand search was carried out for the
following six months (up to May 15th, 2017) in the following journals: British Journal of Oral
and Maxillofacial Surgery, Clinical Implant Dentistry and Related Research, Clinical Oral
5

Page 5 of 19
Implants Research, Journal of Clinical Periodontology, Journal of Cranio- and Maxillofacial
Surgery, Journal of Dental Research, Journal of Oral and Maxillofacial Surgery, Journal of
Periodontal Research, Oral Radiology and Endodontology, Oral Surgery Oral Medicine Oral
Pathology, The Journal of the American Dental Association, Quintessence International.

Data selection

Assessment of search results

The search and screening process was carried out by two independent examiners (MB,CS) to
minimize the potential for reviewer biases. After electronic search all titles, key words and
abstracts were screened. Studies not meeting the inclusion criteria were excluded. All full
texts of the remaining articles were acquired for the second screening. The references of all
selected publications were additionally checked for further relevant data. In cases of missing
or insufficient data the corresponding authors were contacted via e-mail. After detailed full
text examination and agreement between examiners further articles were excluded. All
remaining studies were included in this systematic review. The references were managed with
specific bibliographic software (EndNoteX4, ThomsonReuters®, New York, NY, USA).

Level of Evidence (LoE)

The included studies were judged according to the definition of levels of evidence (LoE) and
overall strength of evidence (SoE) 13.

Data extractions were performed independently by the two reviewers (MB, CS) using data
extraction tables. In cases of disagreements, the data were double checked with the original
data. The following data were extracted from the selected articles

1) authors 2) year of publication 3) title 4) study design 5) primary outcome measures

6) secondary outcome measures 7) surgery technique 8) number of participants 9)
number of cysts 10) Measurements and methods 11) results 12) Follow ups 13)
evidence level

Page 6 of 19
Results

Study characteristics

612 studies were identified from preliminary electronic literature search. Of these, 13 studies
met the inclusion criteria as described in Figure 1. Seven studies between 2008 -2016 aimed
to treat cystic lesions without any grafting method 9-11, 14-17. The other six studies between
2006 -2016 handled treating the lesions with different grafting methods 18-23.

Description of included studies

Descriptions of detailed study characteristics are displayed in Table 1 and 2.

Evidence

The thirteen included studies mainly had a retrospective study design with a Level of
evidence LoE from III to IV. Two of them were designed as prospective studies with a LoE of
II 18, 20, 23.

Cystic lesions

All of the studies included odontogenic cysts like radicular, dentigerous and KCOT’s. Some
studies also reported of eruptions cysts, traumatic bone cysts or aneurysmatic cysts 10, 18, 23.
The number of treated patients ranged from 18 to 322. Only one study considered a
preoperative computed tomography (CT) or magnet resonance imaging (MRI) if the cyst
diameter was >2cm in the dental radiograph 16. The cysts >2cm in diameter were first
decompressed and secondly enucleated. The cysts <2cm in diameter were enucleated. Another
study also adapted the treatment dependent on the diameter of the cyst (< or >2cm) 22. The
cystic lesions >2cm in diameter were filled with ß-TCP (tricalcium-ß-phosphat) + autologous
bone, the cysts <2cm in diameter were filled with ß-TCP. One study included only cysts with
a diameter <5cm 23. They were filled either with ß-TCP or HA (synthetic hydroxyapatite) or
7

Page 7 of 19
not filled. This study indeed measured the decrease of the defect size during the follow-up
period with dental radiographs.

Follow-up periods

The follow-up periods ranged from one to 15 years.

Filling materials

Only one of the included studies compared cystic lesions filled with ß-TCP versus HA or
versus no filling 23. The included studies regarding filling materials report of eggshell-derived
HA, ß-TCP+ PRP (platelet rich plasma), tissue engineered autologous bone or iliac bone.

Outcomes

Descriptions of detailed study characteristics are displayed in Table 1 and 2.

Primary outcome – bone regeneration

Methodology

Methodological approaches for measuring bone regeneration differed from study to study. All
of the included studies used dental radiography (panoramic or dental radiographs) to measure
bone regenerative outcome 2-dimensional. However, none of the included studies performed a
follow-up with 3D scans. Either the increase or decrease of density was analysed or the
diameter of the defect was measured to tell about bone regeneration. The procedure of using
the densitometry was found in three studies 9, 11, 17. One of them used the software called
MCIDTM to evaluate the bone density in converted panoramic radiographs (TIFF format).
They also described the decrease or increase of size of the lesions in the radiographs 17. The
other one invented a standardized protocol to compare different panoramic radiographs. They
used metal markers, 3 mm balls with a distance of 2 mm between them on individual made
vinyl plates, to standardize the pre- and postoperative panoramic radiographs. The
radiographs were digitalized with the program Image J and then they measured the relative
bone density of the pixels in the defect and surrounding bone to tell about increase or decrease

Page 8 of 19
9
. The last study that considered the densitometry analyse used the Nemoceph-NemoStudio,
NX Pro-Nemotec program. They took linear measurements in mm of the cystic lesion
(horizontal, vertical and left/right diagonal) and the distance from the outer boundary of each
line to the point of intersection. Postoperative measurements were taken in the same way to
tell about decrease of size and the density was analysed with the Nemoceph program.

None of the included studies, however, considered different size defects before and after the
treatment or during the follow up period. The defect configuration before and after surgical
treatment was also left unattended by included studies.

At the 12 months observation time point bone formation was measured and judged being half
of the initial defect size 15, 16. In one study, with the follow-up of 6 months outcomes showed a
significant increase in bone density and a decrease of the size of the cyst 17. Measured bone
density showed a significant increase in the mandible compared to the maxilla. One group
measured 97% density increase for treated cysts with a diameter<30mm and 84% for the
treated cysts with a diameter>30mm 9. The mean reduction of the cyst size was about 88,5%
11
.

There were two studies including autogenous bone substitutes as fillers 21, 22. The first one
compared tissue engineered autogenous bone in 11 patients with iliac crest bone in 11
patients. Outcomes revealed insignificant higher density for the tissue engineered bone after
12 months 21. The second study described the use of a mixture of ß-TCP and autogenous bone
for cysts with a diameter >2cm compared to ß-TCP alone for cysts with a diameter <2cm 22.
At the one year follow up the bone density increase was 85% for the ß-TCP with autogenous
bone group and 65% for the ß-TCP group.

Three studies compared ß-TCP with HA for filling 19, 20, 23. In the first study there was a
density increase of 88% after 4 months and 94% after 6 months in the HA group 19. The
second study compared a mixture of ß-TCP+HA+PRP with ß-TCP+HA. The density increase
was 94% for the first group and 47% for the second group after a 6 months follow-up 20. The
third study compared ß-TCP vs. HA vs. no filling of the defect 23. All groups showed no
significant outcomes. The fourth study observed HA vs. an HA from eggshells 18. Outcomes
showed no significant bone density after 3 and 6 months.

Page 9 of 19
Secondary outcomes – clinical parameters

The documentation of secondary outcomes, i.e. wound healing, swelling, pain etc., was only
descriptive in most of the studies 9, 18, 19, 21, 22. Three of them reported of no wound dehiscence
or no significant adverse clinical complications 9, 18, 19. One study observed wound dehiscence
without any signs of acute infection that healed by secondary intention during the follow-up
applying local disinfecting rinses in six of ten patients 21. Fourteen of 152 patients (9.2%)
experienced wound-healing disorders that resulted in partial loss of the filling material in nine
cases (5.9%) in one study 22. But the wounds healed by secondary intention applying local
disinfecting rinses and no major loss of the filler occurred. In three patients (2%) who had
mandibular keratocysts a complete loss of the filling material resulted from secondary
infection. Recurrence rates were reported in one study. Nine KCOT’s, one dentigerous and
one aneurysmatic bone cyst recurred 16.

10

Page 10 of 19
Discussion

This systematic review focused on the impact of the treatment of enucleated jaw cysts on
bony defect regeneration. Specifically we focused on the question whether resulting defects
should rather be filled or left unfilled. In terms of filling we also tried to clarify which is the
suitable filling material for cavity regeneration. Primary outcome parameter was the bony
regeneration measured by means of radiographic imaging (2-and 3D) or radiographic
densitometry. Secondary outcome parameters were clinical and surgical complications as well
as recurrences of the cysts.

Outcomes of the literature search show that the literature lacks knowledge to generally
support one or the other treatment. Furthermore, included studies were very heterogenous in
terms of the used methodology in judging bony defect regeneration after enucleation of jaw
cysts as well as the treated patient cohort and inclusion criteria.

Some studies used the densitometry to assess bone regeneration. For this purpose, panoramic
radiographs were judged with specific software programs. The problem is that the bone
density within the cystic cavity was compared with the surrounding bone on the same side.
This does not allow precise statements. Moreover, within the included studies there are many
different software programs or procedures for assessment and no standardized approach for
densitometry judgment is described. A further problem within choosing densitometry results
as soon as the defect is filled with bone or bone substitute materials. However, the density can
determine the mineralization of the bony defect and cannot make a difference between foreign
bone material and intrinsic bone. Therefore, the results of the included studies which have
chosen this method in combination with filling the defect are so controversial 18-20. Some
describe a higher increase of density during the follow-up comparing HA to β-TCP or
eggshell derived HA 18, 19. Whereas another study described opposite developments in the
increase of density comparing β-TCP to HA 20.

11

Page 11 of 19
The defect size should be considered as one of the most influencing factors for total defect
consolidation. Defects larger than critical size defects (CSD) <1cm3 do not completely and
spontaneously heal no matter how long they are observed 19, 24, 25. It is hypothesized, that there
will be no complete bony regeneration 12, 24, 25, in terms of cystic lesions with a diameter
larger than a CSD that have been left without grafting. Schlegel et al. shows, that in
monocortical critical size defects of 10x10mm in an experimental animal study, the unfilled
defects show incomplete bone regeneration after 52 weeks. On the other hand, defects filled
with autologous bone, showed 100% bone healing after 26 weeks 12. Since the included
studies did not report of the precise defect size its impact stays unclear.

Another influencing factor is defect configuration. It is assumed that defect regeneration is

dependent on the number of intact bony walls. Sufficient stabilization of the blood clot in a
defect with preserved bony walls, bone regeneration from the adjacent bony sites leads to
partial or total defect consolidation. It is well known, that if the lingual and buccal bone is
resorbed or removed during surgery the defect will not completely heal but the formation of
fibrous scar tissue occurs 7, 8. However, it is unclear whether a one hundred percentage defect
consolidation of the jaws in these cases is needed, as long as functional aspects and jaw
stability are guaranteed.

Summarizing the outcome of all included studies (in this part of the review) the authors
concluded that after a mean observation period of 12 months a sufficient bony regeneration
occurred and concluded that defect filling is not necessary. The size of the pre- or
postoperative defect, especially during the follow-up period, was however not investigated as
well as the histological appearance of healed tissues 9-11, 14-17. Outcomes of the included
studies show that in defects after cystectomy a spontaneous bone healing can occur, provided
bony walls and the periosteum are preserved. In these cases the size of the defect as well as
the type of the cyst seems to be not important.

In this review only two studies reported of autologous bone grafts used after enucleation as
defect filler compared to other substitutes 19, 21. However, authors did not compare the same
defect size with different fillers.

Up to date there is no study comparing autologous bone with any kind of bone substitute
material in a prospective comparative treatment approach. The current literature does not
show any studies using xenogenic or allogeneic substitutes for the augmentation of cystic
defects. Bone substitute materials used in the included studies were exclusive synthetic bone

12

Page 12 of 19
substitutes. Concerning bone substitute materials the literature lacks data supporting their use
to fill cavities. Studies with a comparative and prospective design as well as larger patient
cohorts are missing. A final assessment of the use of synthetic grafts can therefore not be
made based on the current clinical studies.

It has to be contemplated, that the methodological approaches of measuring the defect

consolidation after treatment may have an impact. Summarizing the measurement methods in
all included studies (seen in table 1 and 2) to judge bony regeneration the authors concluded
that a 2-dimensional dental radiograph and densitometry gives sufficient information about
the healing process. However, it is hypothesized that measuring bony regeneration by 2D X-
rays or densitometry might lead to a false judgment of bone regeneration. For this purpose 3D
studies concerning defect sizes and defect configuration before and after enucleation as well
as 3D defect regeneration are needed.

The central question of this systematic review cannot definitely be answered due to the poor
data of the literature dealing with this issue. So far it is not clear which procedure leads to a
predictable bony healing after cystectomy. Outcomes of any studies not considering the size
of the defect or comparing different defect sizes treated with different approaches should be
seen critically. Moreover outcomes of any 2D-studies are critical since they cannot give
precise information about defect regeneration. Therefore 3-dimensioal comparative studies
are desperately needed. Also, the question which bone substitute should be used in cases of
filling cannot be answered to date. The usage of autologous bone substitutes should however
be recommended due to its regenerative properties, especially in cases with a defect greater
than a CSD.

Acknowledgements

The authors deny any conflicts of interest related to this study.

13

Page 13 of 19
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Figure 1. Study selection process

15

Page 15 of 19
Table 1 Included studies related to patients with odontogenic jaw cysts. The primary focus was the outcome of bone regeneration after enucleation without
filling Abbreviations: PAN, Panoramic radiograph; RC, radicular cysts; DC, dentigerous cyst; KC, keratocystic cyst; OC, other cysts; D, decompression; E,
enucleation; #, number; CT, computed tomography; MRI, magnet resonance imaging; PS, prospective study; RS, retrospective study; LoE, Level of evidence;
N.a., not applicable.

Author,Yea Study Primary Secondary Technique Participant Cysts Measurement Results Follow up Lo
r Desig outcome outcome s s E
n
Wagdargi S RS density cyst defect 100% 16 16/denti.40%,rad.+odonto.30 PAN/relative mean increase 1,3,6months III
2016 increase decrease enucleation %, Densitometry density/decreas
wihtout e size of cyst
grafting significant after
follow up;
signi.more in
mandible
density;
Rubio 2015 RS bone age/histologic E 18 9 RC, 9DC PAN/relative average 6 months III
regeneratio al results Densitometry reduction size
n 88,47%;66,6%
of patients had
100% bone reg.;
34,4% pateints
65,43% bone
reg.;no
significance in
healing/age or
histological
result
Tkaczuk RS decrease of recurrence >2cm 57 19 KC ,17 DC, 6 RC,10 OC PAN/CT,MRI if Decrease in size 15 years IV
2015 size rate D/<2cm E >2cm for RC;
diameter recurrence 9
KC,1 DC, 1 OC
Manor RS prevalence surgical D#113/E#4 322 N.a. OC,2 KC PAN N.a. 1 year to 5 IV
2012 cysts technique 5 years

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Iatrou 2009 RS surgical characteristics D 17%/E 47 20 DC,5 RC, 5KC, 14 OC PAN 68% cysts were 3,6months, IV
approach of lesions/age 74,5%. developmental , 2years
1 KC reccurence
Ihan 2008 RS bone healing/age E 33 RC,DC,KCOC PAN/relative 97% as 2,6,12 IV
density patients Densitometry surrounding for months
the smaller,
84% for the
bigger size cysts
(>30mm
diameter);
increased age
had negative
influence
Motamedi RS Bone Association 1D,39E 40 DC PAN bone formation 3,6,12month IV
2005 formation with impacted within 6-12 s
teeth months;
relation
impacted
canines
18,wisdom12,10
others

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Table 2 Included studies related to patients with odontogenic jaw cysts. The primary focus was the outcome of bone regeneration after enucleation with filling. Abbreviations:
PAN, Panoramic radiograph; RC, radicular cysts; DC, dentigerous cyst; KC, keratocystic cyst; OC, other cysts; D, decompression; E, enucleation; #, number; CT, computed
tomography; MRI, magnet resonance imaging; AB, autologous bone; SHA, synthetic hydroxyapatite; EHA, eggshell derived HA; TRI, tricalcium-ß-phosphat; PRP, platelet rich
plasma; PS, prospective study; RS, retrospective study; LoE, Level of evidence; N.a., not applicable.

Author,Ye Study Primary Secondary Technique Participan Cysts Measuremen Results Follow up Lo
ar Desig outcome outcome ts ts E
n

Kattamani PS bone clincal E/SHA vs. 20 RC,DC PAN, relative with HA/max at 1,2,3,6mont II
2016 regeneration complications EHA densitometr 24weeks/mean hs
y density similar to
eggshell
3,6months/trabecu
lar at 6months
Shahi PS defect size clincal E/TRI vs. SHA 30 only PAN without graft after 1,2,6 II
2015 decrease complications vs. no graft cysts<5cmdiameter/7 6months not months
3% RC,17% significant but
DC,10%OC biggest decrease of
size/ after 6months
SHA group lowest
decrease not
significant
Kattamani RS radiological VAS,swelling,clinica E/SHA 48 RC,DC PAN, relative 88% after 7days,1,2,6, IV
2013 bone density l complications densitometr 4months/94% after 12months
y 6months

Nagaveni RS bone none E/SHA/TRI+P 20 N.a. PAN, relative Significant for 1,2,4,6mont III
2010 regeneration RP vs. HA/TRI densitometr HA/TRI+PRP (after hs
y 6months 94% vs.
47%)
Pradel RS bone wound E/tissue- 20 11 DC, 6RC, 5KC PAN tissue-eng.AB bone 3,6,12month III
2006 regeneration/bo dehiscence/infecti engineered after 12 months s
ne density ons AB vs. AB higher density, no
(iliac) significance

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Horch RS bone wound E/TRI<2cm 52 22RC,24DC 5KC, 1 OC PAN 1 year after surgery 3,6,12month III
2006 regeneration dehiscence/infecti diameter/>2c 85% TRI+AB s
ons m TRI+AB resorbed/65% TRI

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