Case Report/Clinical Techniques
Repair of Extensive Apical Root Resorption Associated
with Apical Periodontitis: Radiographic and Histologic
Observations after 25 Years
Domenico Ricucci, MD, DDS,* Jos
e F. Siqueira, Jr, DDS, MSc, PhD,† Simona Loghin, DDS,*
and Louis M. Lin, BDS, DMD, PhD‡
Abstract
Introduction: Root resorption is a frequent finding in
teeth with apical periodontitis. In cases of severe apical
periodontitis, root resorption may involve not only
E xternal inflammatory root resorption is a condition associated with periradicular
cementum but also dentin. Resorbed tooth structures
can only be repaired with cementum because stem cells
in the periradicular tissues are not capable of differenti-
ating into odontoblasts. This article reports the repair of
extensive apical root resorption associated with apical
periodontitis 25 years after treatment. Methods: A
51-year-old man presented with pulp necrosis and
symptomatic apical periodontitis in tooth #7. The
periapical radiograph showed a large radiolucent
periradicular lesion and severe root resorption.
Nonsurgical root canal therapy was performed.
Twenty-five years after treatment, a crown fracture
developed, and the tooth could not be restored. The
periapical radiograph revealed complete healing of the
previous apical periodontitis lesion and restoration of
the resorbed root structure. The tooth was removed
and examined histologically. Results: The apical canal
was almost completely filled with a cementumlike tissue
with some strands of entrapped vital uninflamed
connective tissue. Areas of cementum and dentin
resorption in the apical third were repaired by a
combination of cellular and acellular cementum
to which periodontal ligament fibers were attached.
Conclusions: Root resorption caused by apical
periodontitis can be restored almost to its normal
structure after adequate nonsurgical root canal
treatment that succeeded in controlling infection. The
mechanisms behind this process are not clear but
probably involve signaling pathways regulating root
development, cell-cell and cell-matrix interaction, and
morphogens. (J Endod 2014;-:1–7)
Key Words
Apical periodontitis, apical root resorption, cementum
repair, wound healing
From the *Private Practice, Cetraro, Italy; †Department of Endodontics, Est
acio de S
a University, Rio de Janeiro, RJ, Brazil; and ‡Department of Endodontics, New York
University, New York, New York.
Address requests for reprints to Dr Domenico Ricucci, Piazza Calvario, 7, 87022 Cetraro (CS), Italy. E-mail address: dricucci@libero.it
0099-2399/$ - see front matter
Copyright ª 2014 American Association of Endodontists.
http://dx.doi.org/10.1016/j.joen.2014.01.008
JOE — Volume -, Number -, - 2014
inflammation. The large majority of teeth with apical periodontitis exhibit a certain
degree of root resorption (1), which often goes undetected on radiographs (2).
External inflammatory root resorption associated with apical periodontitis is
conceivably initiated by cementum resorption associated with the periradicular
inflammatory response to bacteria or bacterial products leaving the apical or lateral
foramina. Once apical dentin is exposed, the dentinal tubules may permit bacteria
and their products to have another established pathway to contact the inflamed
periradicular tissues, perpetuating inflammation and leading to continued dentin and
cementum resorption (3). If left untreated, the resorptive process can lead to extensive
destruction of the root. Because inflammatory root resorption is usually caused by
bacterial infection of the root canal system, the prognosis of treatment is favorable
provided antimicrobial strategies are applied (4, 5).
Because of obvious ethical limitations, the repair process of apical periodontitis
lesions and root resorption in humans after root canal treatment is by and large
hypothetical. Knowledge is based mostly on observations of repair after tooth extraction
or apical surgery, animal studies, and cross-sectional observations in humans whose
teeth with healed/healing lesions had to be extracted for reasons such as fracture or
prosthetic planning. In this article, we intend to contribute to this type of knowledge
by reporting the radiographic and histologic findings of a tooth exhibiting repair of
extensive apical root resorption associated with apical periodontitis after successful
root canal treatment performed 25 years previously.
Case Report
A 51-year-old man presented with the chief complaint of spontaneous pain in the
anterior maxilla. He also noticed that his maxillary right incisors had become mobile
and tender to chewing. Signs of advanced periodontal disease associated with plaque
and calculus accumulation were present in all quadrants. Periodontal probing revealed
6- to 8-mm deep pockets and bleeding associated with the anterior teeth. Grade 1
mobility was recorded for the anterior teeth, except for the maxillary right lateral
incisor, which showed grade 2 mobility. This tooth had well-adapted mesial and distal
composite restorations and was tender to percussion and palpation. Sensibility tests
(cold, heat, and electric pulp test) gave negative responses for the lateral incisor,
whereas the neighboring teeth responded normally. No sinus tracts were present on
the buccal or palatal gingiva. A periapical radiograph confirmed periodontal bone
loss with abundant calculus accumulation. Periapical radiolucency was present on
tooth #7, measuring 7  8 mm, along with considerable external root resorption
affecting the apical region, particularly on its distal aspect (Fig. 1A). The diagnosis of
Repair of Apical Resorption 1
Case Report/Clinical Techniques

Figure 1. (A) A diagnostic radiograph showing a large apical periodontitis lesion associated with apical root resorption of tooth #7 (inset). (B) Working length
measurement. (C) A postobturation radiograph. (D) Three-year and (E) 15-year follow-up radiographs. (F) A radiograph taken after 21 years 7 months when a
large distal cervical caries lesion was treated. (G) A follow-up radiograph taken after 24 years 5 months. (H) Fracture of the crown occurred after 25 years.
Note thickening of the distal apical area of the root (inset). (I and J) Buccal and distal views of the cleared root.

pulp necrosis with symptomatic apical periodontitis was made for tooth
#7, and the treatment plan included root canal treatment of this tooth
along with scaling and root planing for all quadrants.
After the removal of calculus and plaque with ultrasound and
prophy paste in a rubber cup, the tooth was isolated with a rubber
dam, and the operative field was disinfected with 30% H2O2 and 5%
iodine tincture. All restorative materials and caries were thoroughly
removed. Access preparation was completed, and the working length
was established at approximately 1 mm short of the radiographic
apex (Fig. 1B). A slight distal curvature was present apically. The
root canal was prepared by using Gates-Glidden burs in the coronal
two thirds and hand Hedstr€om files in the apical third. The first file
that bound at the working length was #25. An attempt was made to
prepare an apical stop with a series of instruments of increasing size.
The last instrument used for apical preparation was a #55 Hedstr€om
file. No patency file was used in any phase of root canal instrumentation.
Irrigation was performed with copious amounts of 1% sodium
hypochlorite, which was frequently delivered by a small needle
approximately 3 mm short of the working length. The canal was finally
irrigated with sterile saline solution, dried with sterile paper points, and

2 Ricucci et al. JOE — Volume -, Number -, - 2014


filled with a calcium hydroxide paste (Calxyl Radiopaque; Otto & Co,
Frankfurt, Germany). The paste was placed with a lentulo spiral and
then condensed at the canal orifice with the blunted end of large
paper points. The access cavity was temporized with a reinforced zinc
oxide–eugenol cement (IRM; Dentsply International, Milford, DE).
After 4 weeks, during which the patient had undergone
periodontal treatment, tooth #7 was asymptomatic. The canal was
reaccessed, and the calcium hydroxide paste was carefully removed
by irrigation and instrumentation. The apical preparation was checked
with the last apical file, and after a final rinse with sterile saline, the canal
was dried with sterile paper points. No exudate was observed in the
apical canal; this was confirmed by the fact that a paper point left for
60 seconds in the canal 1 mm short of the working length was
withdrawn completely dry. The canal was obturated with gutta-percha
and sealer using cold lateral compaction (Bioseal; Ogna, Milan, Italy)
(Fig. 1C). The access and the 2 interproximal cavities were restored
with composite materials. A follow-up radiograph taken after 3 years
showed complete healing of the periradicular radiolucency and
improvement of the periodontal bone condition (Fig. 1D). The tooth
was asymptomatic and nontender to percussion and palpation.
Periradicular conditions were stable at the 15-year follow-up, and
apposition of mineralized tissue with remodeling of the previously
resorbed distal apical region of the root could be radiographically
observed (Fig. 1E). However, cervical caries was now present on the
distal aspect of the root (Fig. 1E). The patient decided to postpone
the treatment of the new caries. The carious lesion increased in size after
another 6 years 7 months (21 years 7 months after the root canal
treatment). A radiograph taken after restoration of the cavity revealed
the extent of tooth structure loss on the distal side. Periradicular
structures had remained radiographically normal (Fig. 1F). The
condition was unchanged after 24 years 5 months (Fig. 1G). The patient
presented 7 months after the last follow-up because the crown had
fractured. A radiograph revealed the extent of the fracture. It also
showed that the periradicular conditions were unchanged (Fig. 1H).
The difference of the apical morphology in this radiograph compared
with that in the preoperative radiograph shown in Figure 1A was
noteworthy. Treatment options including restoration with a post
and crown or extraction were carefully explained to the patient. He
decided to extract the tooth and replace it with a removable partial
denture involving other posterior teeth that had been lost over the years.
Permission for histologic examination of the tooth was obtained.
Tissue Processing
Immediately after extraction, the tooth was immersed in 10%
neutral-buffered formalin for 48 hours. Demineralization was
performed in an aqueous solution consisting of a mixture of 22.5%
(vol/vol) formic acid and 10% (wt/vol) sodium citrate for 4 weeks.
The end point was determined radiographically. With a sharp razor
blade, the root was separated from the remaining coronal tissue just
beyond the composite material present at the root canal orifice. The
specimen was washed in running water for 48 hours, dehydrated in
ascending grades of ethanol, cleared in xylene, infiltrated, and
embedded in paraffin (melting point 56 C) according to standard
procedures. Photographs of the root at 90 angles were taken while
the specimen was immersed in the clearing agent (Fig. 1I and J).
With the microtome set at 4–5 mm, longitudinal serial sections
were taken on a mesiodistal plane until the specimen was exhausted.
Particular care was taken to obtain and locate sections passing through
the foramen. Sections were stained with hematoxylin-eosin. Selected
slides were stained with a modified Brown and Brenn technique for
bacteria. Slides were examined under the light microscope.
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Case Report/Clinical Techniques
Histologic Observations
Microscopically, sections through the apical canal and in the area
of the original foramen showed the presence of a mineralized tissue,
which in most sections wrapped the root tip and seemed to completely
fill the apical canal like a well-adapted plug (Fig. 2A and B). However,
other sections revealed small openings containing strands of connective
tissue (Fig. 2C–E). This tissue exhibited lacunae housing cells,
resembling cellular cementum. In some areas, a lamellar structure
could be discerned. The tissue vaguely resembled bone (Fig. 2D and
E). Dark-stained incremental lines could be observed in the thickness
of the newly formed tissue running vertically or horizontally, indicating
successive periods of tissue apposition (Fig. 2A–E).
Observation of the distal apical aspect of the root clearly showed
the extent of the previous severe resorption process, which had
completely destroyed the original cementum layer and most of the
dentinal structure, indicated by a sharp irregular line where dentinal
tubules ended abruptly (Fig. 2H and Fig. 3E). The lost tissue was
replaced by a mineralized tissue, which was atubular in nature and
exhibited lacunae with typical canaliculi. Most of these lacunae housed
cells. The tissue closely resembled cellular cementum (cellular intrinsic
fiber cementum) (Fig. 2G and H and 3A and B). In some areas, the
newly formed tissue exhibited a lamellar structure (Fig. 3D and E).
In some portions of the distal apical root area, some remnants of the
original cementum layer not completely destroyed by the resorptive
process could be observed. These were embedded in the newly formed
cementumlike tissue (Fig. 3A and B). The common feature observed
was that the cementumlike or bonelike tissue filling the irregularities
was lined externally by 1 or more layers of cellular cementum followed
by a layer of acellular cementum (acellular extrinsic fiber cementum) to
which the periodontal ligament (PDL) fibers attached (Figs. 2G and H
and 3A, B, D, and E).
More coronally, the transition to the area not affected by
resorption could be observed with the presence of a cementum layer
partly involved by the process and repaired by new cementum
(Fig. 3C and F) and an intact cementum layer more coronally
(Fig. 3G). Similar features could be observed on the mesial apical
area where the resorbed structures had been repaired by the deposition
of even thicker layers (Fig. 4A–D). Although only acellular cementum
was present apically (Fig. 4A and B), several layers of tissues with
different morphologic characteristics could be observed coronally
(Fig. 4C and D).
The fragments of periodontal tissue remaining attached to the
apical surface at extraction were free from inflammation, showing
only fibroblasts and dense collagen bundles (Fig. 3A, B, D, and G
and Fig. 4B and D). Bacterial staining did not reveal bacteria in the
root canal space or dentinal tubules.
Discussion
Apical periodontitis is a disease caused by intraradicular bacterial
infection usually organized as biofilms adhering to the root canal walls
(6). Dentinal tubules underneath endodontic biofilm communities are
usually penetrated by bacterial cells from the bottom of the biofilm
structure (7, 8). If the cementum layer is lost for any reason (eg,
superficial root resorption because of apical periodontitis lesion or
trauma), dentinal tubule infection or bacterial mediators passing
through tubules may stimulate or sustain inflammation in the PDL
and lead to root resorption (9, 10). Effective antimicrobial
endodontic treatment, including a strategy to disinfect dentinal
tubules (long-term calcium hydroxide dressing), halts the
inflammatory resorptive process, allowing for periradicular healing.
This is what was observed in the present case.
Repair of Apical Resorption 3
Case Report/Clinical Techniques

Figure 2. (A and B) The longitudinal section passing approximately through the center of the canal. Progressive magnifications show that the foramen seems
obliterated by newly formed calcified tissue resembling cementum (hematoxylin-eosin, original magnification 25 and 50). (C–E) Section taken 30 sections
away from that in A. The apical closure is not complete (original magnification 25, 50, and 100). (F) Section close to that in C. Overview (original
magnification 8). (G and H) Progressive magnifications of the distal apical area of the root indicated by the arrows in F. Note that the lost dentin has been
replaced by a tissue that exhibits a lamellar structure and some cellular lacunae. This is lined externally by a darkly stained incremental line and then by a thick
layer of cellular cementum; a thin layer of acellular extrinsic fiber cementum follows to which the PDL attaches (original magnification 50 and 100,
inset 400).

Narrowing of the apical canal by cementum is a common
observation after successful endodontic treatment (11). The histologic
aspects of healing in the foraminal area in the present case fully
confirmed the results of a recent in vivo study (12). In a histologic
analysis of 51 root canal–treated human teeth after long-term follow-
ups, Ricucci et al (12) concluded that it was common to find significant
but incomplete apical closures of the apical part of the root canal with
cementum. Despite the long-term observation periods, no case with
complete cementum closure could be observed. In the present case,
even after a follow-up period of 25 years, apical closure by cementum
seemed complete in most sections, but analysis of serial sections
showed that this plug was actually incomplete, with spaces containing

4 Ricucci et al. JOE — Volume -, Number -, - 2014

 Case Report/Clinical Techniques

Figure 3. (A) A detailed view of the distal apical region of the root just coronally to the area indicated by the arrows in Figure 2F. Two layers of repair cementum,
cellular intrinsic, and acellular extrinsic fiber cementum covering the root dentin surface can be seen. Note the 2 small remnants of the original cementum
embedded in the newly formed calcified tissue (hematoxylin-eosin, original magnification 100). (B) A high-power view of the area demarcated by the rectangle
in A. From right to left: a spicule with some remaining pre-existing dentin (De) and cementum (Ce), a thick layer of cellular intrinsic fiber cementum (CIFC), a
second layer of acellular extrinsic fiber cementum (AEFC), and periodontal ligament (PDL) (original magnification 400). (C) A segment of the distal radicular
region more coronal than that in A (original magnification 16). (D) A detailed view of the area indicated by the upper arrows in C (original magnification 100).
(E) A high-power view of the rectangular area in D. The resorbed dentin appears to have repaired by a bonelike tissue layered externally by acellular extrinsic fiber
cementum (original magnification 400). (F) A high-power view of the area of the distal radicular region demarcated by the rectangle in C. The pre-existing
cementum layer is partly resorbed and repaired by a similar tissue stained less darkly (original magnification 400). (G) A segment of the distal radicular region
more coronal to the area indicated by the lower arrow in C, which was not involved by the resorptive process. Normal-appearing dentin and cementum. The dark
horizontal lines in the cementum are artifacts (folds of the section) (original magnification 100).

strands of vital uninflamed connective tissue (Fig. 2C–E). The formation increased thickening of the canal walls by deposition of cementumlike
of cementumlike tissue in the unfilled apical canal space is similar to the tissue can occur not only in the immature permanent necrotic teeth but
cementumlike tissue formed in many immature permanent teeth with also in the mature necrotic teeth after revitalization/revascularization
necrotic pulp after revitalization/revascularization therapy. Therefore, procedures (13).

JOE — Volume -, Number -, - 2014 Repair of Apical Resorption 5

Case Report/Clinical Techniques

Figure 4. (A) Same section as in Figure 2F (hematoxylin-eosin, original magnification 16). (B) Magnification of the area of the right apical region demarcated
by the upper square in A. Acellular cementum repairing the defect (original magnification 100). (C) Magnification of the area demarcated by the lower rectangle
in A (original magnification 50). (D) A high-power view of the rectangular area in C. Dentin (De) is lined by overgrowing layers of cementum with different
morphologic characteristics, the so-called ‘‘mixed stratified cementum’’ (original magnification 400).

In the presence of periradicular inflammation, resorption of the
apical structure is a common histologic finding, even though the extent
of the root tissue loss may not be sufficient for resorption to be detected
on radiographs (2). In apical periodontitis, some apical alveolar bone,
PDL, cementum, and dentin are destroyed and replaced by inflamma-
tory tissue. After the endodontic infection is effectively controlled by
nonsurgical treatment, inflammation of the periradicular tissues
gradually subsides, and the healing process is started. Although
mesenchymal stem cells retain regenerative potential in the inflamed
periradicular tissues (14), they are not able to differentiate into
specific tissue-committed cells needed for repair and regeneration
(15). Therefore, infection/inflammation must be controlled for wound
healing to occur and stem cells to function.
Wound healing is a complex biological process involving cell-cell
and cell-extracellular matrix cross talk and temporal and spatial
expression of growth/differentiation factors and cytokines as well as
adhesion molecules and other bioactive molecules (16). Periradicular
wound healing requires recruitment of stem/progenitor cells from the
bone marrow and the PDL to differentiate into osteoblasts, PDL cells,
and cementoblasts (17) and usually results in regeneration with
minimal repair because of the availability of progenitor cells.
Healing of external root resorption involving cementum and
dentin caused by apical periodontitis also requires the recruitment of
progenitor cells. Odontoblasts, which produce dentin, can only be
differentiated from the dental pulp stem cells (18) and the stem cells
from apical papilla (19). In mature teeth with apical periodontitis,
the dental pulp is completely destroyed, and the apical papilla no longer
exists. In addition, stem cells/progenitor cells in the PDL and alveolar
bone marrow are not capable of differentiating into odontoblasts
(20, 21). Therefore, the resorbed root dentin caused by the
inflammatory process cannot be regenerated by odontoblasts and
dentin formation.
It has been shown histologically that resorbed root dentin is
repaired by cementum and not by dentin (22, 23). Reparative
cementum is characterized by interposed layers of acellular extrinsic
and cellular intrinsic fiber cementum called ‘‘cellular mixed stratified
cementum’’ (24). Occasionally, the resorbed root surface may be
repaired by bone as dentoalveolar ankylosis or replacement resorption
(10). This type of resorption is usually caused by extensive necrosis of
PDL because of traumatic injury to the teeth (10).
The mechanisms of repair by cementum formation, including the
origin of cementoblasts and the molecules related to their recruitment
and differentiation, remain unclear (25, 26). Cementoblast progenitors
have their origin in the periodontal ligament (usually in a paravascular
location) or the endosteum (27–29). In periradicular tissue healing,
PDL cells adjacent to the affected root area may start to proliferate
and populate the region in which the PDL and cementum were
changed or lost by inflammation. It has been suggested that the
cementum matrix and associated molecules can recruit cementum-
forming stem/progenitor cells in the PDL (25), and dentin matrix might
also be able to signal progenitor cells in the PDL (26) to differentiate
into cementoblasts. Initially, cementoblast progenitors have to be
selected possibly by specific integrins and signaling events (25, 29,
30). Then, the selected cells adhere to the root surface and are
activated by growth factors previously sequestered in the cementum
and dentin matrix and released as a consequence of root resorption

6 Ricucci et al. JOE — Volume -, Number -, - 2014


(3). These factors include bone morphogenetic proteins, transforming
growth factor beta, insulinlike growth factor 1, and epidermal growth
factor (25, 31). Newly formed cementum usually covers areas of the
root where cementum and dentin were lost.
In conclusion, this case report emphasizes that proper control of
root canal infection is essential for healing of the periradicular tissues
after endodontic treatment. The healing process involved active
cementum deposition in an attempt to fill the apical root canal
(although incompletely even after 25 years) and restore the root to
its normal shape with several types and layers of cementum. This type
of root repair could not be observed on the radiographs. It is not clear
why a tooth with severe root resorption caused by apical periodontitis
can be restored almost to its normal root structure after nonsurgical
root canal therapy, but other conditions, such as the resected
root apex after apicoectomy, cannot. Perhaps signaling pathways
regulating root development (32), cell-cell and cell-matrix interaction,
and morphogens (33) are involved.
Acknowledgments
The authors deny any conflicts of interest related to this study.
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Repair of Apical Resorption 7