Short‐term outcomes of lateral extraction socket augmentation using autogenous tooth roots. A prospective observational study

Abstract

Objectives
To assess the short‐term clinical outcomes of lateral augmentation of deficient extraction sockets and two‐stage implant placement using autogenous tooth roots (TR).

Material & Methods
A total of n=13 patients (13 implants) were available for the analysis.
At the time of tooth extraction, each subject had received lateral augmentation using the respective non‐retainable but non‐infected tooth root where the thickness of the buccal bone was <0.5 mm or where a buccal dehiscence‐type defect was present. Titanium implants were placed after a submerged healing period of 6 months and loaded after 20±2 weeks (V8). Clinical parameters (e.g. bleeding on probing ‐ BOP, probing pocket depth – PD, mucosal recession – MR, clinical attachment level – CAL) were recorded at V8 and after 26±4 weeks (V9) of implant loading.

Results
At V9, all patients investigated revealed non‐significant changes in mean BOP (‐19.23±35.32%), PD (0.24±0.49 mm), MR (0.0±0.0 mm) and CAL (0.24±0.49 mm) values, respectively. There was no significant correlation between the initial gain in ridge width and changes in BOP and PD values.

Conclusions
The surgical procedure was associated with stable peri‐implant tissues on the short‐term.

Full text

This article has been accepted for publication and undergone full peer review but has not been
through the copyediting, typesetting, pagination and proofreading process, which may lead to
differences between this version and the Version of Record. Please cite this article as doi:
10.1111/CLR.13633
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DR. KATHRIN BECKER (Orcid ID : 0000-0003-1936-4683)
PROF. FRANK SCHWARZ (Orcid ID : 0000-0001-5515-227X)
Article type : Original Research
Short-term outcomes of lateral extraction socket augmentation using
autogenous tooth roots. A prospective observational study.
Parvini P1, Sahin D2, Becker K1,3, Sader R4, Becker J2, Schwarz F1,2
1 Department of Oral Surgery and Implantology, Carolinum, Goethe University, Frankfurt,
Germany
2 Department of Oral Surgery, Universitätsklinikum Düsseldorf, Düsseldorf, Germany
3 Department of Orthodontics, Universitätsklinikum Düsseldorf, Düsseldorf, Germany
4 Department for Oral, Cranio-Maxillofacial and Facial Plastic Surgery, Medical Center of the
Goethe University Frankfurt, Frankfurt am Main, Germany.
Corresponding address: Frank Schwarz
Department of Oral Surgery and Implantology
Carolinum, Goethe University, Frankfurt, Germany
Tel: +49 69 6301 7924 Fax: +49 69 6301 3829
e-mail: f.schwarz@med.uni-frankfurt.de
Short Title: Extraction socket augmentation
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Key words: clinical study, alveolar ridge augmentation, tooth autotransplantation
Author Contributions
F.S., P.P., R.S. and J.B. conceived the ideas; F.S. performed the surgical procedures; P.P., D.S.,
and K.B. collected and analyzed the data; and P.P., F.S. and R.S. led the writing.
Conflict of Interests and Source of Funding
The authors declare that they have no conflict of interests related to this study.
Source of Funding
The study was funded by a grant of the Deutsche Forschungsgemeinschaft (DFG), Bonn,
Germany.
Abstract
Objectives: To assess the short-term clinical outcomes of lateral augmentation of deficient
extraction sockets and two-stage implant placement using autogenous tooth roots (TR).
Material & Methods: A total of n=13 patients (13 implants) were available for the analysis.
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At the time of tooth extraction, each subject had received lateral augmentation using the respective
non-retainable but non-infected tooth root where the thickness of the buccal bone was <0.5 mm or
where a buccal dehiscence-type defect was present. Titanium implants were placed after a
submerged healing period of 6 months and loaded after 20±2 weeks (V8). Clinical parameters
(e.g. bleeding on probing - BOP, probing pocket depth – PD, mucosal recession – MR, clinical
attachment level – CAL) were recorded at V8 and after 264 weeks (V9) of implant loading.
Results: At V9, all patients investigated revealed non-significant changes in mean BOP (-
19.2335.32%), PD (0.240.49 mm), MR (0.00.0 mm) and CAL (0.240.49 mm) values,
respectively. There was no significant correlation between the initial gain in ridge width and
changes in BOP and PD values.
Conclusions: The surgical procedure was associated with stable peri-implant tissues on the short-
term.
Introduction
The management of extraction sockets has become a topic of major clinical relevance in
contemporary implant dentistry (Avila-Ortiz et al. 2019). In fact, tooth extraction triggers a
cascade of biological events leading to substantial dimensional changes of the alveolar ridge
during the first 6 months of healing (Tan et al. 2012). These changes are more pronounced at the
buccal aspect (Botticelli et al. 2004; Araujo et al. 2015) and intensified in the presence of a
compromised extraction socket. In particular, the presence of a severe bone loss at the time of
extraction resulted in a slower healing and cortication (Ahn & Shin 2008; Bertl et al. 2018) as well
as a greater volume reduction when compared with intact extraction sites (Aimetti et al. 2018).
Moreover, the vertical bone loss was significantly higher at extraction sites exhibiting a thin
buccal bone thickness (< 1 mm) when compared with sites exhibiting a bone thickness of 1 mm or
more (7.5 mm (62%) vs. 1.1 mm (9%), respectively) (Chappuis et al. 2013).
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The results of a recent prospective observational study have indicated that the usage of autogenous
tooth roots (TR) may represent a feasible approach for lateral augmentation of deficient extraction
sockets and two-stage implant placement (Schwarz et al. 2019). In particular, the surgical
procedure included a simultaneous, lateral augmentation of deficient (i.e. thickness of the buccal
bone <0.5 mm or buccal dehiscence-type defects) fresh extraction sockets using the respective
non-retainable but non-infected teeth. After 26 weeks of submerged healing, the change in ridge
width amounted to 4.892.29 mm and allowed for a successful implant placement in all patients
investigated (Schwarz et al. 2019). The basic concept was based on previous findings of a series of
experimental studies indicating that TR have a biological potential to sever as alternative grafts for
localized alveolar ridge augmentation (Schwarz et al. 2016a, 2016b, 2016c).
The aim of the present study was to assess the short-term clinical outcomes of lateral
augmentation of deficient extraction sockets and two-stage implant placement using TR.
Material and Methods
Study design and participants
A total of 15 patients, each exhibiting one non-retainable but non infected tooth attended the
Department of Oral Surgery at the Heinrich Heine University Düsseldorf, Germany and had
received a lateral augmentation of a deficient fresh extraction socket (i.e. either an insufficient
thickness of the buccal bone <0.5 mm or the presence of a buccal dehiscence-type defect) using
the respective TR. After 26 weeks of submerged healing, a re-entry was performed and implants
had been placed at the respective sites. The primary outcome was defined as the crestal ridge
width (mm) (CW26) being sufficient to place an adequately dimensioned titanium implant. The
secondary outcome was the gain in ridge width (CWg), which was calculated as CW26 – CW
measured immediately before augmentation. These data have been published recently (Schwarz et
al. 2019).
At 9 to 20 weeks after implant placement, implant loading was accomplished and clinical baseline
data were recorded. The present analysis focused on the changes in clinical outcomes assessed
after 264 weeks of implant loading. The study outline and the follow-up visits are summarized in
Table 2. Due to lost to follow-up, n=13 patients exhibiting a total of n=13 implants were available
for the present analysis. The patient characteristics and reasons for tooth extraction are presented
in Tables 1a and b. The study protocol was approved by the ethics committee of the Heinrich
Heine University, Düsseldorf and registered via the Internet Portal of the German Clinical Trials
Register (DRKS00009586). Each patient was given a detailed description of the study procedures
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and signed an informed consent before participation. The present reporting considered the
checklist items as proposed in the STROBE statement.
Sample size calculation
Due to the proof-of-principle character of the present observational study and a lack of similar
data in the literature, a sample size calculation was not feasible. However, the initial sample size
of n=15 was considered to be sufficient to allow for a first evaluation of the efficacy (i.e. CWg at
26 weeks) of the presented surgical procedure.
Inclusion and exclusion criteria
Patients were initially included in the study if they presented all of the following conditions: 1)
Age 18 to 60 years, 2) candidate for lateral ridge augmentation, 3) insufficient bone ridge width at
the recipient site for implant placement, 4) sufficient bone height at the recipient site for implant
placement, 5) healthy oral mucosa, at least 3 mm keratinized tissue.
The patients were not included in the study if they presented one of the following conditions: 1)
general contraindications for dental and/or surgical treatments, 2) inflammatory and autoimmune
disease of the oral cavity, 3) uncontrolled diabetes (HbA1c > 7%), 4) history of malignancy
requiring chemotherapy or radiotherapy within the past five years, 5) previous
immunosuppressant, bisphosphonate or high dose corticosteroid therapy, 6) smokers, 7) pregnant
or lactating women (Schwarz et al. 2019).
Surgical procedures
The surgical procedures have been reported in detail previously (Schwarz et al. 2019).
In brief, TR grafts were decapitated at the cemento-enamel junction and the selected root was
separated longitudinally to entirely expose the pulp chamber using a rotating carbide bur under
gentle water (i.e. sterile saline) cooling. Subsequently, all specimens were thoroughly scaled and
root planend using curets to remove all detectable deposits. In addition, any residual pulp tissue
and/ or root canal filling material was removed and the pulp chamber was widened using a round
carbide bur (i.e. sterile saline).
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TR specimens were adapted to match the height and width of the target area and fixed using one to
two titanium osteosynthesis screw (1.5 x 9 mm, Medicon, Tuttlingen, Germany). Periosteal-
releasing incisions were performed to achieve a tension-free wound closure. At 26 weeks,
commercially available titanium implants (Bone Level® Tapered SLActive®, diameter: 4.1 mm,
Institut Straumann AG, Basel, Switzerland) were inserted in an epicrestal position (Visit 6)
without the need for secondary bone grafting procedures. The sutures were removed after 104
days (Visit 7 – V7). The intraoperative measurements of CW values were accomplished to the
nearest 0.25 mm at the most coronal level of the residual buccal bone plate by using a caliper and
have been reported recently.
Prosthodontic procedure
In all patients, a conventional implant loading (Visit 8 – V8) was accomplished at 9 to 20 weeks
after V7 (Table 2). All implants were restored with cemented single metal-ceramic crowns and
bridges and crown margins being located in an epimucosal position. Intraoral radiographs were
taken to ensure the correct position of the respective components and detect residual cement.
Clinical measurements
The following clinical measurements were recorded at V8 and after 264 weeks (Visit 9 – V9) of
implant loading (Table 2) using a pressure-calibrated (20-25g) and colour coded plastic
periodontal probe (Click-Probe® green, Kerr GmbH, Biberach, Germany): 1) plaque index (PI)
(Loe 1967), 2) bleeding on probing (BOP), evaluated as present if bleeding was evident within 30
seconds after probing, or absent, if no bleeding was noticed within 30 seconds after probing, 3)
probing depth (PD) measured from the mucosal margin to the bottom of the probeable pocket, 4)
mucosal recession (MR) measured from the crown margin to the mucosal margin, and 5) clinical
attachment level (CAL) measured from crown margin to the bottom of the probeable pocket. All
measurements were recorded at 6 aspects per implant: mesiovestibular (mb), midvestibular (b),
distovestibular (db), mesiooral (mo), midoral (o), and distooral (do) by one calibrated investigator
masked to the specific experimental conditions (D.S.).
The presence of peri-implant diseases at each implant site was assessed as follows: peri-implant
mucositis: presence of BOP and/ or suppuration with or without increased PD (i.e. V8 to V9);
peri-implantitis: presence of BOP and/ or suppuration with increased PD and presence of bone
loss (i.e. V8 to V9) (Berglundh et al. 2018). No intraoral radiographs were taken, since clinical
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examinations during follow-up did not suggest the presence of peri-implantitis at any implant site
investigated.
Postoperative Care
Postoperative maintenance care included a supramucosal-/ gingival professional implant/tooth
cleaning and reinforcement of oral hygiene. Maintenance care was provided according to
individual needs at V8 and V9.
Statistical analysis
The statistical analysis of the pseudonymised data sets was accomplished using a commercially
available software program (IBM SPSS Statistics 24.0, IBM Corp., Armonk, NY, USA).
Mean values, standard deviations, medians, 95% confidence intervals (CI) and frequency
distributions were calculated for all clinical parameters. The changes (d) in mean values from V8
to V9 were examined with the Shapiro-Wilk test. In a next step, within group comparisons of
dBOP, dPD, dCAL and dKT values were accomplished using the Wilcoxon signed-rank test.
Subsequently, within group changes of dPD and dCAL values were further analysed using the
paired t-test. Linear regression analyses were used to depict the relationship between CWg and
changes in BOP as well as PD values. The chi-square test was employed to compare the incidence
of peri-implant disease between two subgroups. The alpha error was set at 0.05.
Results
Mean CW26 values amounted to 11.232.42 mm (median: 11.5) with a CWg of 4.732.26 mm
(median: 5.0).
Clinical measurements
At V9, all patients investigated exhibited a good level of plaque control, as indicated by mean PI
scores of 0.530.55 (Median: 0.17) at respective implant sites.
Mean and median BOP, PD, MR, CAL, and KT values measured at V8 and V9 are summarized in
Table 3. At V8, mean BOP scores were 65.3837.59% and decreased by 19.2335.32%, thus
resulting in a mean BOP value of 46.1538.01% at V9 (p=0.002, Shapiro-Wilk test; p=0.078,
Wilcoxon signed-rank test). Mean BOP changes were more pronounced at extraction sites
exhibiting a thin buccal bone plate. At V8, mean PD scores were 2.580.30 mm and slightly
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increased by 0.240.49 mm, thus resulting in a mean PD value of 2.830.39 mm at V9 (p=0.123,
Shapiro-Wilk test; p=0.045 Wilcoxon signed-rank test; p=0.094, paired t-test). These changes
were slightly higher at extraction sites exhibiting a buccal dehiscence-type defect (Tables 4 and 5).
All sites investigated did not reveal any noticeable changes in mean MR values at V9.
Accordingly, mean CAL changes amounted to 0.240.49 mm (p=0.123, Shapiro-Wilk test;
p=0.045, Wilcoxon signed-rank test; p=0.094, paired t-test), with slightly higher changes noted at
extraction sites exhibiting a buccal dehiscence-type defect (Fig. 1, Tables 4 and 5). Mean KT
values at V8 were 3.231.16 mm and mainly changed by 0.801.7 mm (p=0.001, Shapiro-Wilk
test; p=0.317, Wilcoxon signed-rank test) at extraction sites exhibiting a buccal dehiscence-type
defect (Tables 4 and 5).
Incidence of peri-implant disease
The frequency distribution of peri-implant disease at V9 is summarized in Table 6. According to
the given case definitions, the incidence of peri-implant mucositis and peri-implantitis amounted
to 76.92% and 0.0%, respectively. The chi-square test pointed to an independency between both
subgroups and the incidence of peri-implant disease (p=0.118) (Table 6).
Regression analysis
At V6, mean CWg values amounted to 4.892.29 mm (median: 5.00; 95% CI: 3.56; 6.21)
(Schwarz et al. 2019).
The linear regression analysis failed to reveal a significant correlation between CWg and changes
in BOP (Coef: 0.321, R2=0.103, p=0.285) and PD values (Coef: 0.167, R2=0.028, p=0.585,
respectively (Figs. 2a and b).
Discussion
The present study aimed at investigating the short-term clinical outcomes of lateral augmentation
of deficient extraction sockets and two-stage implant placement using TR. After a follow-up
period of 44 weeks (i.e. at 264 weeks after loading), all patients investigated revealed non-
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significant changes in mean BOP (-19.2335.32%), PD (0.240.49 mm), MR (0.00.0 mm) and
CAL (0.240.49 mm) values when compared with V8. In this context, it must be emphasized that
the present observational study had a proof-of-principle character and may therefore not have the
statistical power to rule out significant within group changes for the presented clinical outcomes.
Moreover, it must be emphasized that the relatively high BOP scores noted at V8 may mainly be
attributed to a traumatic tissue injury caused by the crown/ bridge insertion at respective implant
sites. Accordingly, the BOP changes at V9 reflect a healing of the peri-implant soft tissue
following completion of the implant supported restorations.
The remaining mean BOP scores at 44 weeks are basically within the range of the short-term data
on peri-implant health or disease noted at native (non-augmented) implant sites (Schwarz et al.
2017). In particular, in a cross-sectional analysis of 238 patients exhibiting a total of 512 two-
piece implants, the diagnosis peri-implant mucositis (case definition: BOP on at least one aspect of
the implant but no changes in the radiographic bone level) was commonly noted in all implant age
groups investigated. At the implant level, its frequency amounted to n=25 at 1-12 months of
follow-up, n=157 at 12-48 months and n=32 at >48 months, respectively (Schwarz et al. 2017). In
contrast, a meta-analysis (n= 10 studies) of short-/ mid-term (1–3 years) and long-term (>3 years)
data on the effects of various lateral ridge augmentation procedures on peri-implant health or
disease did not reveal any major changes in BOP scores over time (i.e. follow-up of 1 to 10 years).
The calculated weighted mean differences amounted to −10.02% (95% CI: −22.23; 2.21) and
failed to reach statistical significance (Sanz-Sanchez et al. 2018). Similar findings with respect to
BOP changes were also observed when different timings (i.e. simultaneous or staged) and surgical
procedures (i.e. different types of barrier membranes, growth factors, chin blocks with or without
resorbable membranes) were compared (n = 6; WMD = −3.36; 95% CI [−12.49; 5.77]; p = .471).
These procedures were also associated with stable PD scores (n = 6; WMD = −0.051; 95% CI 0.0;
0.0]; p = .726) and marginal bone levels (n = 6; WMD = 0.062; 95% CI 0.0; 0.527]; p = .284)
(Sanz-Sanchez et al. 2018), thus corroborating the findings of the present study.
At the time being, this is the first clinical study which aimed at investigating the application of TR
for a lateral augmentation of deficient extraction sockets. However, a recent prospective case
series (4 patients) reported on the clinical performance of TR grafts (derived from impacted teeth)
for lateral alveolar ridge augmentation and staged implant placement (Pohl et al. 2017). The
clinical follow-up at 2 years revealed mean PD scores of 1.7 mm (range: 0 to 3.5 mm) in the
absence of BOP (Pohl et al. 2017). This was also supported by the outcomes of an initial human
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case report, pointing to healthy and stable (PD values of 3 to 4 mm) peri-implant tissue conditions
at 8 months following lateral ridge augmentation using TR and staged implant placement
(Schwarz et al. 2016b).
When further analysing the present regression analysis, it was also noted that the initial gain in
ridge width was not significantly correlated with changes in BOP and PD values. While this
observation may support recent findings of a less pronounced resorption of TR when compared
with AB grafts (Schwarz et al. 2018), it remains unclear to what extent graft remodeling will
affect both TR groups and subsequently clinical outcomes in the mid- and long-term.
A major limitation of the present clinical analysis was the impossibility to further assess the
biological integration of the inserted implants at TR grafted sites. However, previous preclinical
animal studies provide histological evidence that a true osseointegration was established by the
interposition of woven bone between residual TR fragments and the implant surface (Schwarz et
al. 2016a, c). The resulting removal torque values were comparable to those values noted at
titanium implants that were placed following lateral ridge augmentation using autogenous bone
blocks (Becker et al. 2017).
In conclusion and within its limitations, the present clinical study revealed that the surgical
procedure was associated with stable peri-implant tissues on the short-term.
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Fig. 1.Representative clinical outcomes at V9.
a. Situation at re-entry in the region of former tooth 25 where TR had been
used for the augmentation of a thin buccal bone plate (Visit 6).
b. Healthy peri-implant soft tissue conditions as indicated by the absence
of BOP.
c. Situation following implant bed preparation in the region of former tooth
23, where TR had been used for the augmentation of a buccal
dehiscence-type defect (Visit 6).
d. Clinical situation immediately following gentle probing pointing to
healthy and stable peri-implant soft tissues.
Fig. 2 Linear regression plots to depict the relationship between CWg and dBOP/
dPD values.
a. dBOP
b. dPD
Figure legends

Tables
Table 1a.
Patient characteristics (refers to Visit 7).
Patient age
50.0±7.5 years; range: 34 to 58 years
female/ male
n = 7/6
subgroup - insufficient bone thickness
n = 8
subgroup - dehiscence-type defect
n = 5
Table 1b.
Reasons for tooth extraction and numbers (refers to Visit 2).
substantial loss of the clinical crown
n= 10 (6 with endodontic treatment)
fractured teeth
n = 2
advanced periodontal destruction due to
occlusal trauma
n = 1

Table 2.
Study design and follow up visits (D=day; W=week).
Visit 1
Visit 2
Visit 3
Visit 4
Visit 5
Visit 6
Visit 7
Visit 8
Visit 9
Enrollment
Surgery
SR
R/ IP
SR
IL, CM
CM
D0
D10
W4
W13
W26
D104
post V6
W9-202
post V7
W264
post V8
Visit 1: patient enrollment
Visit 2: lateral ridge augmentation using TR
Visit 3: SR=suture removal
Visits 4/ 5: follow-up visits
Visit 6: R=re-entry/ IP=implant placement
Visit 7: SR
Visit 8: IL=implant loading; CM=clinical measurements of baseline data
Visit 9: CM=clinical measurements of follow-up data
Table 3.
a. Clinical parameters measured at V8 (n=13 patients).
BOP
PD
MR
CAL
KT
Mean
65.38
2.58
0.00
2.58
3.23
SD
37.59
0.30
0.00
0.30
1.16
Median
67.00
2.67
0.00
2.67
3.00
95% CI
42.6;88.1
2.40;2.76
0.00;0.00
2.40;2.76
2.52;3.93
b. Clinical parameters measured at V9 (n=13 patients).
BOP
PD
MR
CAL
KT
Mean
46.15
2.83
0.00
2.83
3.53
SD
38.01
0.39
0.00
0.39
1.33
Median
33.00
2.92
0.00
2.92
3.00
95% CI
23.18;69.13
2.59;3.07
0.00;0.00
2.59;3.07
2.73;4.34

Table 4.
Changes (d) in clinical parameters between V8 and V9 (n=13 patients).
dBOP
dPD
dMR
dCAL
dKT
TR
mean
-19.23 ± 35.32
0.24 ± 0.49
0.0 ± 0.0
0.24 ± 0.49
0.30 ± 1.1
median
0.0
0.17
0.0
0.17
0.0
95% CI
-40.57; 2.11
-0.04; 0.54
0.0; 0.0
-0.04; 0.54
-0.36; 0.97
Cohen`s d
-0.54
0.50
-
0.50
0.27
p value
0.078*
0.094**
-
0.094**
0.317*
Within group comparison V8 - V9: * Wilcoxon signed-rank test; **paired t-test
Table 5.
a. Patients exhibiting extraction sockets with a thin buccal bone plate (<0.5 mm) (n=8).
dBOP
dPD
dMR
ΔdCAL
dKT
TR
mean
-27.13 ± 39.82
0.15 ± 0.56
0.0 ± 0.0
0.15 ± 0.56
0. 0 ± 0.0
median
0.0
0.17
0.0
0.17
0.0
95% CI
-60.42; 6.17
-0.31; 0.63
0.0; 0.0
-0.31; 0.63
0.0; 0.0
b. Patients exhibiting extraction sockets with a buccal dehiscence-type defect (n=5).
dBOP
dPD
dMR
dCAL
dKT
TR
mean
-6.60 ± 25.35
0.39 ± 0.34
0.0 ± 0.0
0.39 ± 0.34
0.80 ± 1.7
median
0.0
0.50
0.0
0.50
0.0
95% CI
-38.08; 24.88
-0.03; 0.83
0.0; 0.0
-0.03; 0.83
-1.42; 3.02

Table 6.
Crosstabulation of subgroup and incidence of peri-implant disease at V9.
Diagnosis
Total
0
1
Subgroup
Thin bone
Count
3
5
8
% within Subgroup
37.5%
62.5%
100.0%
Dehiscence type defect
Count
0
5
5
% within Subgroup
0.0%
100.0%
100.0%
Total
Count
3
10
13
% within Subgroup
23.1%
76.9%
100.0%
Diagnosis: 0 = healthy; 1 = peri-implant mucositis; p=0.118, Chi-square test.

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