Jan Lindhe. Clinical Periodontology
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MUCOGINGIVAL THERAPY – PERIODONTAL PLASTIC SURGERY •
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646 • CHAPTER
27
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CHAPTER 28
Regenerative Periodontal
Therapy
THORKILD KARRING, JAN LINDHE AND PIERPAOLO CORTELLINI
Introduction
indications
Regenerative surgical procedures
Reliability of assessments of periodontal
regeneration
Periodontal probing
Radiographic analysis and re-entry operations
Histologic methods
Periodontal wound healing
Regenerative capacity of hone cells
Regenerative capacity of gingival connective
tissue cells
Regenerative capacity of periodontal ligament
cells
Role of epithelium in periodontal wound healing
Root resorption
Regenerative procedures
Grafting procedures
Root surface biomodification
Growth regulatory factors for periodontal
regeneration
Guided tissue regeneration (GTR)
Clinical application
Conclusions
INTRODUCTION
At tooth risk assessment in periodontal patients, the
presence of sites with a residual pocket depth 6 mm
after active treatment plays a significant role in pre-
dicting future periodontal destruction (Haffajee et al.
1991, Grbic St Lamster 1992, Claffey & Egelberg 1995).
Thus, an important goal of periodontal therapy is to
obtain a reduced pocket depth after treatment in order
to arrest further disease progression. Usually, this goal
can be accomplished by non-surgical therapy in pa-
tients with moderate periodontitis, whereas in ad-
vanced cases, particularly in the presence of intrabony
defects and furcations, the treatment must be supple
-
mented with periodontal surgery. A fundamental ob-
jective of periodontal surgery is to provide access for
proper instrumentation and cleaning of the root sur-
face, but in addition, most surgical procedures result
in the elimination or the reduction of the soft tissue
component of the periodontal pocket. Traditionally,
the elimination of deep pockets is achieved by
gingivectomy or apical displacement of raised tissue
flaps, sometimes associated with bone contouring. In
recent years, however, the use of regenerative proce-
dures aimed at restoring the lost periodontal support
has become more common.
Indications
Periodontal treatment, either surgical or non-surgical,
results in recession of the gingival margin after heal-
ing (Isidor et al. 1984). In advanced cases of periodon
-
titis, this may lead to poor esthetics in the front areas
of the dentition, in particular when applying surgical
procedures including bone contouring for the eradi-
cation of bone defects. Treatment of such cases with-
out bone contouring, on the other hand, may result in
residual pockets inaccessible to proper cleaning dur-
ing post-treatment maintenance. These problems can
be avoided or reduced by applying regenerative sur-
gical procedures by which the lost periodontal attach
-
ment in the bone defects can be restored. Thus, the
indication of applying regenerative periodontal ther-
apy is often based on esthetic considerations, besides
the fact that the function or long-term prognosis of the
treated teeth may be improved.
Localized gingival recession and root exposure
may
represent an esthetic problem to the patient, and
REGENERATIVE PERIODONTAL THERAPY • 651
often it is associated with root sensitivity. Such a situ
-
ation represents an indication to apply regenerative
periodontal therapy to obtain root coverage in order
to improve esthetics and reduce root sensitivity. Suc-
cessful root coverage implies regeneration of the at-
tachment apparatus on the exposed root surface in-
cluding cementum with inserting collagen fibers and
alveolar bone as well as an esthetically acceptable
restoration of the anatomy of the mucogingival com-
plex.
Another indication for regenerative periodontal
therapy is furcation involved teeth. The furcation area
is often inaccessible to adequate instrumentation and
frequently the roots present concavities and furrows
which make proper cleaning of the area after resective
surgery impossible. Considering the long-term results
and complications reported following treatment of
furcation involvements by traditionally resective ther-
apy (Ramp et al. 1975, Biihler 1988), the long-term
prognosis of furcation involved teeth can be improved
considerably by successful regenerative periodontal
therapy.
Case reports also exist demonstrating that "hope-
less" teeth with deep vertical defects, increased tooth
mobility or through and through furcations can be
successfully treated with regenerative periodontal
therapy (Gottlow et al. 1986). However, controlled
clinical trials or serial case reports presenting a reason
-
able predictability of treating such advanced cases are
not available.
Regenerative surgical procedures
Regenerative periodontal therapy comprises proce-
dures which are specially designed to restore those
parts of the tooth-supporting apparatus which have
been lost due to periodontitis. Regeneration is defined
as a reproduction or reconstruction of a lost or injured
part in such a way that the architecture and function
of the lost or injured tissues are completely restored
(
Glossary of Periodontal Terms
1992). This means that the
attachment of the tooth has been regenerated when
new cementum with inserting collagen fibers has
formed on the detached root surface, while regenera-
tion of the periodontal supporting apparatus (perio-
dontium) also includes regrowth of the alveolar bone.
Procedures aimed at restoring lost periodontal sup-
port have also been described as "reattachment" or
"
new attachment" procedures.
The term "reattachment" was used to describe the
regeneration of a fibrous attachment to a root surface
surgically or mechanically deprived of its periodontal
ligament tissue, whereas the term new attachment"
was preferred in the situation where the fibrous at-
tachment was restored on a root surface deprived of
its connective tissue attachment due to the progres-
sion of periodontitis. Research findings, however; in-
dicate that there is no difference regarding the possi-
bility of restoring a connective tissue attachment,
whether this has been lost because of periodontal
disease or mechanically removed (Nyman et al. 1982,
Isidor et al. 1985). Therefore, it was suggested that the
term "new attachment" should be used to describe the
formation of new cementum with inserting collagen
fibers on a root surface deprived of its periodontal
ligament tissue, whether or not this has occurred be-
cause of periodontal disease or by mechanical means,
and that the term "reattachment" should be confined
to describing the reunion of surrounding soft tissue
and a root surface with preserved periodontal liga-
ment tissue (Isidor et al. 1985).
Periodontal regeneration has been reported follow-
ing a variety of surgical approaches involving root
surface biomodification, often combined with coron-
ally advanced flap procedures, the placement of bone
grafts or bone substitute implants, or the use of or-
ganic or synthetic barrier membranes (guided tissue
regeneration). However, many cases that clinically are
considered successful, including cases with signifi-
cant regrowth of alveolar bone, may histologically
show an epithelial lining along the treated root surface
instead of deposition of new cementum (Listgarten &
Rosenberg 1979).
Successful regeneration is assessed by periodontal
probing, radiographic analysis, direct measurements
of new bone and histology. Although histology re-
mains the ultimative standard in assessing true peri-
odontal regeneration, periodontal probing, direct
bone
measurements and radiographic measurements
of
osseous changes are used in the majority of studies
of
regenerative therapy (Reddy & Jeffcoat 1999).
At the American Academy of Periodontology
World
Workshop in Periodontics in 1996, the fulfill
ment of
the following criteria was required in order for a
periodontal regenerative procedure to be consid
ered
as a therapy which can encourage regeneration:
•
Human histological specimens demonstrating for-
mation of new cementum, periodontal ligament
and bone corona] to a notch indicating the apical
extension of the periodontitis affected root surface
•
Controlled human clinical trials demonstrating im-
proved clinical probing attachment and bone
•
Controlled animal histological studies demonstrat-
ing formation of new cementum, periodontal liga-
ment, and bone.
In addition, however, it seems reasonable to require
that a regenerative procedure is based on a biological
concept which on the basis of current knowledge
about periodontal wound healing can explain why the
treatment results in periodontal regeneration.
652 • CHAPTER 28
RELIABILITY OF ASSESSMENTS OF
PERIODONTAL REGENERATION
In most studies on the effect of regenerative periodon-
tal surgery, the outcomes are evaluated by probing
attachment level measurements, radiographic analy-
sis or re-entry operations. However, such methods are
not reliable for documentation of a true gain of attach
-
ment (i.e. a new connective tissue attachment in an
area coronal to the attachment level before treatment).
Periodontal probing
The inability of periodontal probing to determine ac-
curately the coronal level of the connective tissue
attachment has been demonstrated by several inves-
tigators (Listgarten et al. 1976, Armitage et al. 1977,
Van der Velden & de Vries 1978). It is known from these
studies that in the inflamed periodontium, the probe
does not stop precisely at the coronal level of the
connective tissue attachment. Usually it penetrates
half a millimeter or more into the connective tissue,
surpassing the transition between the apical extension
of the dento-gingival epithelium and the coronal level
of connective tissue attachment. After therapy, when
the inflammatory lesion is resolved, the probe tip
tends to stop coronal to the apical termination of the
epithelium. Following treatment of intrabony defects,
new bone may form so close to the tooth surface that
the probe cannot penetrate (Caton & Zander 1976).
Thus, a gain of probing attachment level (PAL) follow-
ing therapy does not necessarily mean that a true gain
of connective tissue attachment was accomplished.
More likely it is a reflection of improved health of the
surrounding soft tissues which offer increased resis-
tance to probe penetration. (For a detailed discussion
on errors inherent in clinical probing of periodontal
pockets see Chapter 18.)
Radiographic analysis and re-entry
operations
Regeneration of bone tissue within intrabony defects
following regenerative therapy is often documented
by
measurements made on radiographs obtained in a
standardized and reproducible manner and/or as-
sessed in conjunction with a re-entry operation.
Analysis of radiographs before and after therapy and
inspection of the treated area during a re-entry opera
-
tion can certainly provide evidence of new bone for-
mation. However, such "bone fill" does not document
formation of new root cementum and a new periodon-
tal ligament. In fact, it was demonstrated by Caton &
Zander (1976) and Moscow et al. (1979) that despite
the fact that bone regeneration had occurred adjacent
to the root in intrabony defects, a junctional epithe-
lium was interposed between the newly formed bone
and the curetted root surface. This means that radio-
graphic analysis and assessments of bone formation
by re-entry operations are unreliable methods for the
documentation of new attachment formation.
Histologic methods
In several studies healing is analyzed in histologic
sections of block biopsies obtained after various forms
of regenerative periodontal therapy. Histologic analy-
sis is the only valid method to assess the formation of
new attachment, but it requires that the location of the
attachment level prior to therapy can be assessed with
a certain accuracy.
h1
a few studies histologic reference
notches were placed in the apical extent of calculus
deposits, identified on the root surface at the time of
surgery (Cole et al. 1980, Bowers et al. 1989b,c). Usu
-
ally, however, a reference is obtained by producing a
notch in the root surface at the level of the reduced
bone height. Although such a notch may not reflect
the exact position of the periodontitis-involved root
surface prior to treatment, it is considered an adequate
landmark for the assessment of new attachment (Isi-
dor et al. 1985).
PERIODONTAL WOUND HEALING
Regeneration of the periodontium must include the
formation of new cementum with inserting collagen
fibers on the previously periodontitis-involved root
surfaces and the regrowth of the alveolar bone. How-
ever, whether regrowth of alveolar bone should al-
ways be considered a requirement for success follow-
ing regenerative periodontal surgery is a matter of
discussion. The basis for this discussion is that also in
a normal non-periodontitis affected dentition in the
presence of bone dehiscenses and fenestrations, a fi-
brous attachment may exist without opposite bone
(
see Fig. 1-74).
In 1976, Melcher in a review paper suggested that
the type of cell which repopulates the root surface after
periodontal surgery determines the nature of the at-
tachment that will form. After flap surgery the curet-
ted root surface may be repopulated by four different
types of cell (Fig. 28-1):
1.
Epithelial cells
2.
Cells derived from the gingival connective tissue
3.
Cells derived from the bone
4.
Cells derived from the periodontal ligament.
Previously, in most attempts to restore lost tooth sup-
port, particular attention was directed towards the
regeneration of the alveolar bone. In order to examine
the relationship between the re-establishment of a
REGENERATIVE PERIODONTAL THERAPY • 653
Fig. 28-1. Following flap surgery, the curetted root sur-
face may be repopulated by (1) epithelial cells, (2) gin-
gival connective tissue cells, (3) bone cells, or (4) peri-
odontal ligament cells.
Fig. 28-2. Following flap elevation, the buccal bone, in-
cluding a part of the interradicular and interproximal
alveolar bone, is removed without injuring the connec-
tive tissue attachment on the root surface.
Fig. 28-3. Microphotograph of
specimen 8 months following
bone
removal (a). A connective tis
sue
attachment is re-established
(
arrows). Bone regeneration is neg-
ligible and is confined to the notch
(N) in the root surface. (b) Higher
magnification of the newly
formed
bone in the notch area (N).
connective tissue attachment to the root surface and
the
regrowth of alveolar bone, an investigation was
carried
out in dogs (Nyman & Karring 1979). After
elevation of
mucoperiostal flaps, the marginal 5-7 mm of the buccal
alveolar bone of each experimental tooth
was removed (
Fig. 28-2). During this procedure, care
was taken to
minimize the mechanical injury to the connective tissue
attachment on the root surface. A
notch, serving as a landmark for the histologic meas-
urements, was prepared in the root surface at the level
of the surgically reduced bone crest. After 8 months of
healing, the animals were sacrificed. Histologic analy
sis
demonstrated that although a connective tissue
attachment was re-established consistently on the
roots,
the amount of bone regeneration varied widely.
In some
roots, bone regrowth was negligible (Fig.
654 • CHAPTER 28
Fig. 28-4. Schematic drawing showing the four experimental conditions (a-d) under which experimental teeth were
extracted and reimplanted in their own sockets.
28-3), whereas in others the bone had regenerated to
its normal level. These results demonstrated that the
amount of bone regrowth is unrelated to the re-estab
-
lishment of a connective tissue attachment.
Another experiment was carried out in monkeys (
Lindhe et al. 1984), in order to examine whether the
presence of bone may stimulate the formation of a new
connective tissue attachment. Mandibular and maxil
-
lary incisors were extracted and reimplanted in their
own sockets under the following four experimental
conditions (Fig. 28-4):
1.
Non-root planed teeth were reimplanted into sock-
ets with normal bone height
2.
Teeth, root planed in their coronal portion, were
reimplanted into sockets with normal bone height
3.
Non-root planed teeth were reimplanted into sock-
ets with a reduced bone height
4.
Teeth, root planed in their coronal portion, were
reimplanted into sockets with reduced bone height.
Histologic examination after 6 months of healing re-
vealed that a fibrous reunion was established in areas
where, at the time of reimplantation, the periodontal
connective tissue attachment was retained. However,
in areas, where the periodontal ligament tissue was
removed, the epithelium had always migrated to the
apical extension of root instrumentation (Fig. 28-5).
These results of healing occurred irrespective of the
presence or absence of bone, indicating that the estab
-
lishment of a connective tissue attachment is unre-
lated to the presence of alveolar bone.
Using orthodontic appliances, Karring et al. (1982)
tilted maxillary second and third incisors in labial
direction in dogs. Subsequently, these teeth were
moved back to their original position. During the
same time the contralateral incisors were moved to a
labially deviated position. The orthodontic appliances
were then used to retain the teeth in these positions
for a period of 5 months before sacrifice of the animals.
Histologic analysis demonstrated that in all experi-
mental teeth, the apical termination of the junctional
epithelium was at the cemento-enamel junction. In the
teeth which were retained in their labially displaced
position, the level of the alveolar bone was reduced to
a
position about 4.5 mm apical to the cemento-enamel
junction (Fig. 28-6a), while in the teeth which were
moved back to their original position, the alveolar
bone crest was located at a normal level relative to the
cemento-enamel junction (Fig. 28-6b). This experi-
ment demonstrated that in the presence of a normal
connective tissue attachment, bone may be resorbed
or regenerated by orthodontic forces. Thus, the experi
-
ments described above indicate that the re-establish-
ment of a connective tissue attachment to the root
surface and the regeneration of the alveolar bone are
not related to each other.
The use of bone grafts in regenerative periodontal
therapy is based on the assumption that the promo-
tion of bone regrowth may also induce cells in the bone
to produce a new cementum layer with inserting col-
lagen fibers on previously periodontitis-involved root
surfaces. However, histologic studies in both humans
and animals have demonstrated that grafting proce-
dures often result in healing with a long junctional
epithelium rather than a new connective tissue attach
ment (Caton 8z Zander 1976, Listgarten & Rosenberg
1979, Moscow et al. 1979).