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Deciduous Tooth Pulp Autotransplantation for the Regenerative Endodontic

Treatment of Permanent Teeth With Pulp Necrosis: A Case Series

Article in Journal of Endodontics · February 2022

DOI: 10.1016/j.joen.2022.01.015

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CASE REPORT/CLINICAL TECHNIQUES
Zafer C. Cehreli, DDS, PhD,
Deciduous Tooth Pulp Gizem Erbas Unverdi, DDS,
PhD, and Elif Ballikaya, DDS, MS
Autotransplantation for the
Regenerative Endodontic
Treatment of Permanent Teeth
With Pulp Necrosis: A Case
Series

ABSTRACT
SIGNIFICANCE
Introduction: In young individuals, deciduous tooth pulp might be used as a natural, biologic
scaffold for the regenerative endodontic treatment (RET) of young permanent teeth with Autotransplantation of
necrotic pulps and apical periodontitis. The present case series demonstrates the clinical and deciduous tooth pulp as a
radiographic outcomes of a novel RET using deciduous pulp autotransplantation in biologic scaffold could be a
traumatized, necrotic young permanent incisors. Methods: Five previously traumatized viable approach in the
maxillary incisors of four 8- to 11.5-year-old patients were treated with a RET protocol that regenerative endodontic
used 2.5% NaOCl irrigation and placement of calcium hydroxide dressing in the first visit. After treatment of young permanent
4 weeks, the intracanal medication was removed, and the whole pulp tissue harvested from teeth with pulp necrosis.
the neighboring maxillary deciduous canine was transplanted into the disinfected root canal
without induced apical bleeding. Following placement of a mineral trioxide aggregate coronal
barrier, the access cavities were restored with acid-etch resin composite. The root canals of
donor primary canines were filled with calcium hydroxide-iodoform paste and were restored
as with the permanent incisors. Results: Three patients were followed-up for 24 months, and
1 patient for 12 months. All teeth demonstrated radiographic evidence of complete periapical
healing, slight increase in dentinal wall thickness, and continued apical closure in the absence
of clinical symptoms. A positive response to cold test was obtained in 1 incisor at 12 months
and 2 at 24 months. Conclusions: Based on 12- and 24-month clinical and radiographic
findings, the present cases demonstrate a favorable outcome of a RET protocol using de-
ciduous pulp autotransplantation in young permanent incisors with pulp necrosis. (J Endod
2022;-:1–6.)

KEY WORDS
Autologous transplantation; deciduous tooth; pulp; regeneration; regenerative endodontics;
revascularization

Two decades ago, revascularization was introduced as a biologically based treatment for regenerating
From the Department of Pediatric
the pulp-dentin complex in immature teeth with pulp necrosis1–3. Since then, there has been an Dentistry, Faculty of Dentistry, Hacettepe
exponential growth in the number of clinical and preclinical publications in the field of regenerative University, Ankara, Turkey
endodontics4,5, leading to a better understanding of the nature and behavior of the revitalized tissue Address requests for reprints to Dr Zafer
within the root canal, as well as factors associated with favorable and unfavorable treatment outcomes3. C. Cehreli, Department of Pediatric
The widely used terms “revascularization” and “revitalization” refer to regenerative endodontic Dentistry, Hacettepe University Faculty of
procedures (REPs), which aim to facilitate ingrowth of new, vascularized tissue within the disinfected root Dentistry, 06100 Ankara, Turkey.
E-mail address: zcehreli@gmail.com
canal space following delivery of stem cells from the apical papilla (SCAP) and cells from other periapical 0099-2399/$ - see front matter
tissues by induced apical bleeding3. After the root canal is passively filled with the blood, the clot that
Copyright © 2022 American Association
forms in the canal space serves as a biologic scaffold for cell growth and differentiation6. The blood clot of Endodontists.
also contains several blood-derived growth factors capable of attracting other stem cells from periapical https://doi.org/10.1016/
tissues that can initiate ectopic deposition of mineralized tissues (ie, bone, cementum) within the root j.joen.2022.01.015

JOE  Volume -, Number -, - 2022 Deciduous Tooth Pulp Autotransplantation 1

canal, and cause progressive narrowing of the
canal space, which might complicate future
endodontic treatment, if needed7–9. Histologic
data from both animal studies and human
teeth following traditional REPs using blood
clot as a scaffold have shown histologic
evidence of a new repair tissue, rather than a
newly regenerated pulp-dentin complex9–11.
The relatively more recent introduction of REPs
using autologous platelet concentrates (eg,
platelet-rich plasma, platelet-rich fibrin) as
biologic scaffolds have also resulted in similar
histologic findings of repair tissue containing
mineralized and fibrous connective tissues
rather than a newly regenerated pulp10,11.
Altogether, these outcomes have led authors
to describe this traditional treatment approach
as “guided endodontic repair”3 or “cell-free
regenerative endodontic therapy”12.
Recently, dental pulp
autotransplantation has been described as a
new regenerative endodontic treatment
approach in a case series of 3 single-rooted,
mature premolars, using the pulp tissue
harvested from third molars that were
scheduled for extraction13. The 12-month
clinical and radiographic findings showed
advanced periapical healing and favorable
blood flux on Doppler assessment in 18- to 40-
year-old patients. Transplanted pulp can serve
as an optimal scaffold, owing to its feasibility
and great potential for cell growth and
differentiation without the risk of host
rejection13. The same potential applies to
deciduous tooth pulp, which is a rich source of
highly proliferative stem cells and growth
factors in a natural scaffold containing
vasculature14. Deciduous teeth are readily
available as a biologic scaffold in young
individuals suffering pulp necrosis in immature
permanent teeth as a consequence of trauma
and dental caries. Moreover, the donor
deciduous tooth can be successfully
preserved by endodontic treatment until
natural exfoliation. To the best of our
knowledge, deciduous tooth pulp has not
been used as a scaffold in REPs. This case
series presents the autotransplantation of
deciduous tooth pulp as a scaffold for the
biologically based endodontic treatment of
traumatized, necrotic young permanent teeth,
and the 12- to 24-month clinical and
radiographic outcomes.
MATERIALS AND METHODS
Patients
Case 1 was a healthy, 10.5-year-old boy who
was referred to a pediatric dentistry
department for the endodontic and restorative
treatment of traumatized maxillary incisors.
Reportedly, he had experienced a fall accident
2 Cehreli et al.
5 months earlier, but refused to visit a dentist.
Clinical examination revealed complicated
crown fractures of left central and lateral incisor
in the absence of pain on palpation and
percussion, swelling, sinus tracts, and mobility.
The fractured incisors did not respond to cold
test or electric pulp tests (EPTs), whereas the
contralateral and neighboring teeth responded
positively to both tests. Radiographic
examination showed slight periapical
radiolucency (Fig. 1). A common diagnosis of
pulp necrosis and asymptomatic apical
periodontitis was made.
Case 2 was an 11.5-year-old girl, who
was admitted to the pediatric dentistry
department for the management of crown
discoloration after the treatment of a traumatic
dental injury. The parents reported that the
child had a fall accident that led to a crown
fracture 8 months earlier, and the local dentist
performed emergency treatment with mineral
trioxide aggregate (MTA) pulpotomy and resin
composite restoration. Over time, the patient
had several episodes of spontaneous pain, but
did not visit the dentist. The parents decided to
seek treatment because of slight crown
discoloration. Clinically, the tooth was free of
mobility, pain, and swelling, and did not
respond to cold and EPTs. There was no pain
on palpation and percussion. Radiographic
examination confirmed the history of
pulpotomy, along with slight periapical
radiolucency and advanced apical closure
(Fig. 1). A diagnosis of pulp necrosis and
asymptomatic apical periodontitis was made.
Case 3 was a healthy 8-year-old boy
with a history of untreated complicated crown
fracture of a maxillary right central incisor due
to a fall accident 6 months earlier. His tooth
showed the same clinical and radiographic
findings as case 1, with slight periapical
radiolucency (Fig. 1). A diagnosis of pulp
necrosis and asymptomatic apical
periodontitis was made.
Case 4 was an 8-year-old boy with a
history of complicated crown fracture after
being hit by a swing 4 months earlier.
Reportedly, the local dentist tried to remove
the pulp, but could not complete the
procedure because of low patient compliance
and scheduled the patient for root canal
therapy, but the patient refused to attend
further treatment. The clinical and radiographic
findings and diagnosis were the same as with
case 3 (Fig. 1). The endodontic access was
exposed due to premature partial loss of
temporary cement.
Considering the varying levels of
incomplete apical closure of the affected teeth
along with the availability of neighboring intact
donor primary teeth, a regenerative
endodontic treatment protocol using
deciduous pulp autotransplantation was
planned. Informed consent was obtained from
all patients and parents after explaining and
discussing the possible outcomes of treatment
and the treatment plan in case of failure.
Autotransplantation Protocol
All teeth underwent a common, 2-visit
regenerative endodontic treatment protocol.
At the first appointment, the incisors requiring
treatment were isolated with a rubber dam
after local anesthesia, and endodontic access
was obtained with water-cooled high-speed
diamond burs. The root canal length was
estimated by conventional radiographic
method. The root canals were gently irrigated
with 20 mL freshly prepared 2.5% NaOCl using
closed-end and side-vented needles placed 2
to 3 mm below the apex and without any
instrumentation. Following copious irrigation
with sterile saline, the root canals were dried
with sterile paper points, and a calcium
hydroxide paste was loosely packed into the
root canal approximately 2 mm below the
apex. The access cavities were sealed with
approximately 4 mm of conventional glass
ionomer cement and the patients were recalled
after 4 weeks.
At the second (autotransplantation)
appointment, a disinfection and isolation
protocol, based on a previously described
report to acquire sterile pulp samples15, was
performed before operative procedures.
Accordingly, the patients first rinsed with
0.12% chlorhexidine mouthwash for 30
seconds. Then, the injection sites for the local
anesthetic (2% mepivacaine, Citanest;
AstraZeneca, London, UK) involving the
maxillary permanent incisors and primary
canine were scrubbed with 10% povidone
iodine for 2 minutes. A thick rubber dam sheet,
previously disinfected by thorough scrubbing
with 10% povidone iodine for 2 minutes was
placed with punched holes exposing only the
permanent incisor and primary canine, and
secured with sterile rubber dam clamps. Then,
the interface of the tooth and rubber dam were
sealed with light-cured resin barrier (Top Dam;
FGM Dental, Joinville, SC, Brazil). The isolated
crown surfaces were polished with a with a
presterilized medium-grit pumice in sterile
saline, followed by scrubbing with 2%
chlorhexidine for 2 minutes, and 5,25% NaOCl
for 2 minutes.
The permanent incisors were re-
accessed with high-speed, water-cooled
sterile diamond burs after disinfection of the
tooth crown. The calcium hydroxide dressing
was removed by gentle irrigation with 10 mL
sterile saline. The irrigation was completed with
a 60-second application of passive ultrasonic
JOE  Volume -, Number -, - 2022
FIGURE 1 – Radiographic outcome of deciduous pulp autotransplantation treatment. For each case pair, the left and right radiographs show preoperative and final follow-up findings,
respectively (cases 1, 2, and 3: 24 months and case 4: 12 months). Arrows demonstrate physiologic root resorption of pulpectomized primary canines along with progressive resorption
of the root canal paste.
irrigation (PUI) using an Endoultra Ultrasonic
activator (Vista Apex, Racine, WI) with the tip of
the ultrasonic activator placed 2 mm below the
apical level, followed by a final flush with saline
to remove the remnants of calcium hydroxide
loosened by PUI. The root canals were dried
with sterile paper points, and then gently
irrigated with 20 mL of 17% EDTA15. No apical
bleeding was induced before
autotransplantation. Then, a mechanical pulp
exposure, in the size of an endodontic access
cavity, was created on the donor primary
maxillary canine crown using a separate, high-
speed water-cooled sterile diamond bur. A
new, presterilized barbed broach was used to
remove the whole pulp (coronal 1 radicular
pulp), to provide enough pulp volume to fill the
permanent root canal. Thereafter, the whole
pulp was quickly released from the broach
using a sterile tweezer, and gently inserted into
the recipient root canal using disinfected gutta-
percha cones, lubricated with the blood
volume from the primary canine root canal. In
case 1, both maxillary canines were used as
donors for the treatment of permanent central
and lateral incisors, because the whole pulp
volume of a deciduous canine could suffice for
1 permanent root canal. A non-staining MTA
coronal barrier (Neo MTA 2.0; NuSmile,
Houston, TX) was placed over the deciduous
JOE  Volume -, Number -, - 2022
pulp scaffold and sealed with a thin layer of
flowable light-cured glass ionomer cement
(Ionoseal; VOCO, Cuxhaven, Germany) to
prevent MTA from washout during subsequent
adhesive procedures. The coronal level of the
autotransplant, together with the blood volume
transferred from the primary canine(s)
determined the thickness of the MTA barriers.
Accordingly, the coronal barriers were thicker
in case 1 compared with cases 2, 3, and 4,
which had a thickness of approximately 3 to
4 mm.
The access cavities were restored with
acid-etch resin composite (Filtek Ultimate; 3 M/
ESPE, St Paul, MN). Before removal of the
rubber dam, the primary root canal was filled
with a calcium hydroxide paste with iodoform
(Calciplast Forte; Cerkamed, Stalowa Wola,
Poland), and the access cavity was restored as
with the recipient incisor. No medications were
prescribed. Following oral hygiene instructions,
the patients were scheduled for clinical and
radiographic follow-up visits at 3 and
6 months, and thereafter, every 6 months.
RESULTS
A total of 5 maxillary incisors (4 central and 1
lateral) were treated with the regenerative
endodontic treatment protocol using
deciduous pulp autotransplantation. Cases 1,
2, and 3 were followed for 24 months and case
4 for 12 months. All teeth showed complete
periradicular healing in the absence of clinical
symptoms. Cases 1, 2, and 3 showed a slight
increase in root wall thickness, with the
resultant canal space being similar in size to
that of adjacent vital teeth. There was no visible
sign of root canal narrowing or obliteration
(Fig. 1). Compared with cases 1, 2, and 3, case
4 showed greater thickening of the apical half
of root walls, but the pulp space was similar to
the adjacent vital incisor as with cases 1, 2,
and 3 (Fig. 1). All teeth showed a blunt
narrowing of the apical region (with case 3 to a
lesser extent), rather than a typical, conical
apical closure pattern. All 3 teeth in case 1 and
case 2 responded to cold test at 12 and
24 months, respectively, whereas the
remaining teeth did not respond to cold test or
EPTs at any recall period. The donor primary
canines were free of clinical symptoms and
showed radiographic evidence of physiologic
root resorption along with resorption of the
calcium hydroxide-iodoform paste (Fig. 1).
DISCUSSION
Although current REPs using the so-called
revascularization or revitalization technique
Deciduous Tooth Pulp Autotransplantation 3
with induced apical bleeding cannot
regenerate lost pulp tissue, they have been
used widely for the endodontic treatment of
immature permanent teeth with pulp necrosis
because of their relative simplicity compared
with apexification procedures and their
favorable patient- and clinician-based
outcomes, which include periapical healing,
tooth survival and function, and radiographic
root development3. It should be cautioned that
the potential of the new, vascularized repair
tissue to promote continued root development
is limited by the extent of damage on Hertwig’s
epithelial root sheath and apical papilla
induced by trauma or apical periodontitis,
leading to unpredictable treatment
outcomes12,16,17. Such unpredictability also
includes the commonly reported problem of
progressive root canal obliteration8,18,19,
which might lead some clinicians to prefer
apexification procedures that offer similar
survival rates20–22. In fact, teeth receiving REPs
with induced apical bleeding may require
retreatment much earlier than those receiving
apexification treatment, and their failure rates
increase more rapidly over the time23. These
findings call for an urgent switch to REPs that
do not use the blood clot from induced apical
bleeding as a scaffold. Based on published
literature, autologous platelet concentrates
might seem to be the most suitable alternative
scaffold to the blood clot, and when used
without prior apical bleeding, platelet
concentrates can induce root growth and
innervation with significantly less risk for
progressive root canal obliteration8. However,
platelet concentrates are costly and less
patient-friendly, especially in children and
adolescents.
The feasibility of using autologous
deciduous tooth pulp as a biologic scaffold for
regenerative endodontic treatment has been
shown previously in the animal model24. This
case series presents the first clinical use of
deciduous pulp autotransplantation and its 12-
to 24-month outcomes. From a clinical
standpoint, deciduous pulp
autotransplantation may offer several benefits
in children and young patients, because it is
readily available and does not require apical
bleeding or burdensome collection of
peripheral blood to obtain platelet-derived
scaffolds. Moreover, the entire treatment can
be accomplished in the clinical setting without
the need for additional equipment and/or
laboratory procedures24. As a biologic
scaffold, deciduous pulp contains a rich
population of stem cells that have a higher
proliferation rate than those from adult human
teeth25. Deciduous pulp also contains multiple
growth factors, such as transforming growth
factor-beta, fibroblast growth factor-2,
4 Cehreli et al.
platelet-derived growth factor, and vascular
endothelial growth factor in a natural
microenvironment. Dental pulp is not the main
source of growth factors, but should ideally
contain them if used as a scaffold and source
of cells in a regenerative therapy. Since early
phases of the so-called revascularization
technique, dentin has been traditionally used
as an intrinsic source of growth factors
liberated by EDTA conditioning, but this
common clinical practice has not necessarily
led to the histological demonstration of primary
dentin or true parenchymal pulp tissue in vivo.
It is, thus reasonable to benefit from the
additional source of growth factors naturally
present in the pulp autotransplant with high
potential to promote dentinogenesis, guide the
phenotypic expression of odontoblast
progenitors, and facilitate differentiation13.
These growth factors can also attract stem
cells and promote stem cell proliferation by
promoting angiogenesis in the initial stages of
healing26. In addition, the ability of deciduous
dental pulp stem cells to establish
vascularization is more robust than that of
dental pulp stem cells27. Thus, in the presence
of an open apical foramen, deciduous dental
pulp stem cells may help establish vasculature
to ensure sufficient nutrient supply for tissue
regeneration24,26,27. With an autotransplant
inherently containing all those components, it
might also be possible to observe a faster rate
of tissue regeneration compared with
techniques that use cells, scaffolds, and
growth factors separately. In our case series,
cases 3 and 4 did not respond to cold test at
recall periods. Positive response to vitality tests
is a desirable clinician-based outcome of
regenerative endodontic treatment3, but may
not be detected in every case owing to the
absence of nerve regeneration. In such cases,
it is more appropriate to demonstrate pulp
vitality by Doppler ultrasound evaluation, which
provides proof of revascularization13.
In the present case series, the 1- and 2-
year radiographic observation of the increase
in root wall thickness was markedly slow and
modest compared with a routine case of
conventional revascularization with typically
greater potential for progressive, uncontrolled
root wall thickening28. Deciduous tooth pulp
has a very low tendency for calcification29,
which as a biologic scaffold may have exerted
a limiting, regulatory effect on the secretory
activity of cells that differentiate within the root
canal space. Coupled with the lack of induced
apical bleeding, which prevents the acute influx
of non-SCAP cells with aggressive mineralizing
properties7, this might have favorably limited
any uncontrolled, progressive calcific tissue
deposition over time. Accordingly, it might be
possible to speculate that the new vital tissue
regenerated as a result of homing of SCAP and
the internal source of autotransplanted
deciduous pulp stem cells, which might have
differentiated into a pulp-like tissue over time. It
is worth mentioning herein that the common
radiographic finding of apical closure pattern
showing blunt narrowing rather than
regenerating to a conical apical closure was
considered highly unlikely related to the
potency of the autotransplantation procedure,
because blunt narrowing has already been
documented as a common apical closure
pattern after regenerative endodontic
therapies30.
For the autotransplantation procedure,
maxillary deciduous canines were used as a
source for primary tooth pulp, because they
offer a reasonably large pulp volume that can
be easily harvested from a single root canal. In
addition, their proximity to the recipient
maxillary permanent incisors allows for the
same anesthesia and isolation procedures.
Even in cases with little or no physiologic root
resorption, the volume of the deciduous canal
space may not be sufficient to fill a permanent
root canal. For this reason, we used the whole
pulp (ie, we used both the coronal and
radicular pulp volume), which was sufficient to
fill most of the canal space from apical to the
level of one-third the coronal MTA plug with
some voids. To fill the voids, we used the
fresh blood volume transferred from the
donor primary canines. Transferring blood
from other root canals has already been
described as a practical and successful
method in REPs31,32. In our cases, the
bleeding was initiated by the apical separation
of primary pulp tissue, and not by
instrumentation beyond the apex, as would
be typically performed in conventional
revascularization. Thus, there should be a
lesser chance that the apical bleeding would
introduce cells from the periapical region with
mineralizing properties that might cause
progressive canal obliteration over time. In
situations in which the pulp volume is not
enough or when the pulp does not entirely fit
the root canal of a permanent tooth, the pulp
transplants can be positioned near the apex
for better nutrient supply and the remaining
canal space can be filled with the blood from
the donor primary tooth. Finally, in deciduous
pulp autotransplantation, the donor primary
teeth can be successfully retained with
endodontic therapy until natural exfoliation33,
with the frequently encountered, progressive
resorption the root-filling paste having no
significant effect on treatment outcomes34.
Chemical agents used for the treatment
of immature necrotic teeth should be selected
not only based on their antimicrobial
properties, but also on their ability to provide a
JOE  Volume -, Number -, - 2022
stable and safe environment for stem cell
survival at the periradicular area. It has been
demonstrated that calcium hydroxide, even in
a thick consistency of 100 mg/mL are
conducive to SCAP survival and proliferation,
whereas such high concentrations of
antibiotics used in REPs have a detrimental
effect on SCAP survival35. It should be noted
that removal of calcium hydroxide from the
root canal is difficult, and currently there is no
clinical protocol that can provide complete and
predictable removal of calcium hydroxide form
the root walls, particularly from the apical
region. It has been shown that PUI might
enhance calcium hydroxide removal,
regardless of the solution of activation35. In the
present case series, PUI was used with sterile
saline, and activation of the latter was made
2 mm below the apical level to prevent apical
extrusion.
Although case reports and series
possess a low impact in determining the
efficacy of a given treatment method36, they
can demonstrate clinical observations with
considerable translational potential into
clinical studies as well as to the development
of clinical practice37,38. The present case
series suggests that deciduous pulp may
have a potential for use as a biologic scaffold
in the regenerative endodontic treatment of
necrotic, open-apex and nearly closed-apex
young permanent teeth, by using a patient-
friendly, uncomplicated autotransplantation
protocol without the need to extract the
donor deciduous tooth. However, these early
observations must be supported by long-
term randomized trials before its routine use
can be advocated.
ACKNOWLEDGMENT
The authors deny any conflict of interest.

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6 Cehreli et al. JOE  Volume -, Number -, - 2022

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