Periodontology 2000, Vol.

19, 1999, 115-137

Printed in Denmark . All rights reserved

Coavrinht 0 Munkspaard 1999

PERIODONTOLOGY 2000
ISSN 0906-6713

THORKILD
KARRING& PIERPAOLO
CORTELLINI

Regenerative therapy furcation defects

The invasion of the furcation areas of multirooted
teeth by periodontitis represents a serious complication in periodontal therapy. The furcation area is
often inaccessible to adequate instrumentation,
and frequently the roots present concavities and
furrows which makes proper cleaning of the area
impossible (8). As long as the pathological process
is extending only a minor distance (<5 mm; degrees I and I1 involvement) into the furcation area,
further progress of the disease can usually be prevented by scaling and root planing provided that a
proper oral hygiene program is established after
treatment (93). In more advanced cases (5-6 mm;
degree I1 involvement) the initial cause related
treatment is frequently supplemented with surgery
involving contouring of the interradicular bone
(osteoplasty) or reduction of the tooth prominence
at the furcation entrance by grinding (odontoplasty), in order to reduce the horizontal extension of
the furcation involvement (51). In cases where the
involvement extends deeper into the furcation area
(>5 mm; degree I1 involvement) or a through and
through defect (degree I11 involvement) has developed, tunnel preparation or root resection has
been advocated as the choice of treatment (18, 75).
However, both of these latter treatments involve a
risk of complications on a long-term basis. Following tunnel preparation, caries frequently develops
in the furcation area and root resected teeth often
present non-periodontal complications, although
controversial reports exist regarding the long-term
results of these treatment modalities (12, 34, 44-46,
66).
Considering the complexity of current techniques
for the treatment of furcation problems, and in the
view of the long-term results and complications reported following treatment of advanced furcation involvements by traditionally resective therapy, pre-

dictable regeneration of the periodontium at furcation-involved sites would represent a considerable

progress in periodontics.

Regeneration of furcation defects

Periodontal regeneration is the restoration of the
tooth-supporting tissues including cementum, periodontal ligament and alveolar bone over a previously
diseased root surface. Clinically, successful regeneration at furcation sites is determined as the elimination or reduction of the horizontal and vertical
components of the lesion (that is, gain of clinical
probing attachment level and bone fill), but the conclusive evidence of true regeneration can only be
achieved by histological means.
Regeneration of furcation defects has been reported following a variety of surgical approaches involving root surface conditioning, often combined
with coronally advanced flap procedures, the placement of bone grafts or bone substitute implants, or
the use of organic or synthetic barrier membranes
(guided tissue regeneration). However, many cases
that clinically are considered successful, including
cases with significant regrowth of alveolar bone, may
histologically show an epithelial lining along the
treated root surface instead of deposition of new cementum (64).
At the American Academy of Periodontology
World Workshop in Periodontics in 1996 (log), the
presence of the following criteria was considered in
evaluating clinical procedures for their capacity to
promote regeneration:
human histological specimens demonstrating formation of new cementum, periodontal ligament
and bone coronal to a notch in the root indicating
the apical extension of the periodontitis-affected
root surface;
controlled human clinical trials demonstrating

115

Karring & Cortellini

Fig 1. Microphotograph of furcation 6 weeks after grafting

with iliac crest marrow (A). The furcation is completely
filled with bone (B), but ankylosis (AN)and root resorption (RS) can be seen. The area showing ankylosis and
resorption is seen at higher magnification in B. OC: osteoclasts.

improved clinical probing attachment and bone

levels;
controlled animal histological studies demonstrating formation of new cementum, periodontal
ligament and bone.
It is, however, also reasonable to require that a regenerative procedure be based on a biological concept which, in accordance with current knowledge
about periodontal wound healing, can explain why
the treatment may result in periodontal regeneration.

Wound healing in furcation defects

It was suggested by Melcher ( 7 2 ) that the type of cell
that repopulates the periodontitis affected root surface after periodontal surgery determines the nature
of the attachment that will form. After surgical intervention in the periodontal region, the detached and
cleaned root surface may be repopulated by four dif-

116

ferent types of cell: 1)epithelial cells, 2 ) gingival connective tissue cells, 3 ) bone cells and 4) periodontal
ligament cells.
Healing of furcation defects following flap surgery
including bone grafting was studied in experiments
in monkeys (32, 33, 77). These studies, where various
types of bone graft were placed in furcation defects,
revealed that only in iliac bone marrow grafts did
bone forming cells survive transplantation. The use
of iliac bone marrow grafts almost consistently resulted in bone fill in the experimental defects, but
healing was frequently accompanied by ankylosis
and root resorption (Fig. 1). It was suggested that it
was the bone-forming cells, transferred into the defects with the grafts, that were inducing root resorption (32). Jaw bone grafts (Fig. 2) or xenografts
placed in the furcation defects did not actively contribute to bone formation but served as a scaffold
for bone growth from the interradicular bone septum (33, 77). Root resorption was never observed in
these defects, but frequently the bone grafts were not
reached by the new bone growing out from the host

Regenerative therapy: furcation defects

Fig. 2. Microphotograph (A) demonstrating a bifurcation

defect 3 weeks after grafting with autogenous cancellous
jaw bone ( G ) . New bone has invaded the defect, and the
bone grafts have exerted an osteoconductive function.
Epithelium (arrows) has migrated into one side of the defect. The higher magnification of the midportion of the
defect (B)shows that new bone has formed around the
bone grafts (G),which have lost their vitality, as indicated
by the empty osteocyte lacunae.

bone. The bone grafts often persisted in the furcation as isolated particles surrounded by cementum or a cementum-like substance (Fig. 3). At
the time they were killed, the monkeys used in these
studies were injected with Indian ink into the vascular system, thereby allowing the course of the blood
vessels to be determined in thick cleared histological
specimens representing various stages of healing
(Fig. 4). It appeared from the course of the blood
vessels, that the major portion of newly formed
tissue in the furcation defects originated from the
periodontal ligament at the bottom of the defect,
whereas only a small portion originated from the
bone. It was suggested that the overwhelming ingrowth of periodontal ligament tissue inhibited bone
formation in the furcation and that the new cementum on the root surface in the bifurcation, including the cementum-like substance observed
around the implanted bone particles, was produced
by periodontal ligament cells. Thus, the results of
these studies suggested that the key cells in periodontal regeneration are the periodontal ligament
cells.

The key role of periodontal ligament cells in periodontal regeneration was supported by the results of
a number of studies in experimental animals, evaluating the regenerative capacity of each of the periodontal tissues involved in periodontal wound healing (52-55, 80). It was found that root resorption
rather than new attachment occurred if the detached
root surface was repopulated by cells derived from
bone or gingival connective tissue. A new connective
tissue attachment with cementum and inserting collagen fibers was formed only when periodontal ligament cells were allowed to repopulate the root surface. However, apical migration of epithelium reduced the coronal gain of attachment, evidently by
preventing repopulation of the root surface with
periodontal ligament cells.
The conclusive evidence that the progenitor cells
for new attachment formation are residing in the
periodontal ligament was provided in studies in
monkeys in which titanium dental implants were
placed in contact with retained root tips, whose periodontal ligament served as a source for cells which
could populate the implant surfaces during healing

117

Karring & Cortellini

Fig. 3. Microphotograph of a healed bifurcation defect following transplantation of non-vital bone grafts (A). The
grafts (G) have not been reached by bone formation from
the interradicular septum (S) but occur as isolated particles surrounded by cementum(arrows).Cementum (C)
and new connective tissue attachment formation have
taken place along the entire circumference of the bifurcation. The isolated bone grafts (G) with newly formed cementum on the surface are seen at high magnification in
B.

(13, 14, 107). Microscopic analysis revealed that a

distinct layer of cementum with inserting collagen
fibers had formed on the surfaces of these implants
that were placed in contact with the periodontal
ligament of the retained root tips. The inserting collagen fibers, often oriented perpendicularly to the
surface of the implant, were running across a ligament space and were embedded in the opposite
bone (Fig. 5). Control implants (Fig. 61, placed without contact with retained roots, healed consistently
with the characteristic features of osseointegration
(i.e., direct contact between bone and the implant
surface).

Regenerative treatment of
furcation defects
In the evaluation of the outcome of regenerative
surgery, it is important to be able to determine the
type of healing that results. A gain in clinical attachment level has become widely accepted as one of the

118

primary clinical endpoints of regenerative periodontal surgery. However, clinical attachment levels
do not accurately assess the coronal level of connective tissue attachment to the root surface. While a
gain in clinical attachment may represent regeneration, it may also represent resolution of tissue inflammation and reformation of tissue collagen,
fibers causing an increased resistance to probe penetration (65).
Re-entry procedures, which involves a second surgical entry of the regenerative site, provide a very accurate assessment of bone fill at the treated sites but
do not distinguish bone that is attached to the root
surface via junctional epithelium or a periodontal
ligament (64).
Histological evaluation remains the only reliable
method of determining the nature of the attachment
apparatus following regenerative procedures. It has
been suggested that only regeneration coronal to a
notch placed at the apical extent of calculus, identified on the root surface at the time of surgery,
should be considered valid proof of regeneration in

Regeneratiue therapy: furcatio n defects

Root conditioning
It was suggested by Stahl (98) that demineralization
of the previously periodontitis-involved root surface,
exposing the collagen of the dentin, would facilitate
periodontal regeneration. The effect of root surface
conditioning by topical application of acids, primarily citric acid, was evaluated in both experimental
animals and in humans.
Biological concept. The biological concept is that
the acid treatment causes demineralization of the
root planed dentin, hereby exposing collagen fibrils
of the dentin matrix. It is assumed that this exposure
of collagen fibrils may facilitate adhesion of the
blood clot to the root surface and favor migration of
fibroblasts and that the exposed collagen fibrils of
the dentin matrix may interdigitate with newly
formed collagen fibrils in the adjacent healing
tissues (35, 39, 91, 97).

Fig. 4. Cleared specimen from a one-week-oldbifurcation

defect treated with autogenous bone grafts. Judgingfrom
the course of the blood vessels, the granulation tissue in
the defect has developed mainly from the periodontal
ligament (arrows) and only to a minor extent from the
interradicular septum (IS).

human subjects. Using this rigorous criterion, it has

been conclusively demonstrated that periodontal regeneration can occur on a periodontally diseased
root surface (9, 10, 22, 99, 100). Usually, however, a
reference is obtained by producing a notch in the
root surface at the level of the reduced bone height.
Although such latter notch may not reflect the exact
position of the apical extent of the periodontitis-involved root surface prior to the treatment, it is considered adequate since no difference was observed
between the potential for new attachment formation
on a previously periodontitis-involved root surface
and on a root surface deprived of its periodontal
attachment by surgical means (50).
It should be emphasized that regenerative surgery
does not represent a method to treat periodontitis.
The goal of regenerative surgery is to alter or heal the
anatomic defects produced by active periodontitis.
Therefore, prior to regenerative treatment, the periodontal infection must be treated by eliminating the
pathogenic microflora by conventional therapeutic
measures.

Animal studies. Several studies in experimental

animals have demonstrated increased amounts of
new connective tissue attachment in furcation defects following acid conditioning compared with
non-acid-treated controls (6, 26, 79). Likewise, Caffesse et al. (151, Claffey et al. (20) and Wikesjo et
al. (108) reported improved attachment formation
in furcation defects in dogs treated with citric acid
or tetracycline root conditioning and coronally positioned flaps. The results, however, were often associated with root resorption. On the basis of the
observation in a study in monkeys and dogs by
Hinge et al. (58) that 9 of 13 furcation defects
healed with new attachment when the flaps were
coronally positioned while none of seven with normal placement developed new connective tissue
attachment, it was concluded that adequate coverage of the furcation area by coronally sutured flaps
is critical for new attachment to occur following
citric acid conditioning. Wikesjo et al. (1081, however, observed that, with increasing distance from
the periodontal ligament, the frequency of root resorption and ankylosis increased. This finding supports the view that the most important factor for
the establishment of a new connective tissue
attachment is a predictable repopulation of the
root dentin surface with cells derived from the
periodontal ligament rather than the quality of the
root surface. This view is in accordance with current knowledge about periodontal wound healing
that periodontal ligament cells are essential for
true periodontal regeneration.

119

Karring & Cortellini

Fig. 5. Microphotograph of a titanium implant placed in

contact with retained root tips (A).A distinct cementum
layer (arrows) and a periodontal ligament (PL) in continuity with that on the root (R) is visible adjacent to the
implant surface. B.A high magnification in polarized light
of the periodontal ligament formed around an implant. A
cementum layer (arrows) with Sharpeys fibers is present

at the implant surface. The Sharpeys fibers are in continuity with principal fibers, oriented perpendicularly to
the implant surface, and which are running across the
ligament space (LS) and are inserting in the opposite bone
(B) like at natural teeth. A vascular plexus (V), similar to
that seen around natural teeth, also seems to have
formed.

Human studies. New connective tissue attachment

following citric acid demineralization of a previously
periodontitis affected root surface was demonstrated
histologically in humans (22). Histological evidence
of a new connective tissue attachment and bone formation was found coronal to reference notches
placed in the apical extent of calculus, identified on
the root surface at the time of surgery. However, despite the histological evidence of regeneration and
the encouraging results in experimental animals following citric acid root conditioning, no controlled
clinical trial on furcation defects has documented
any advantage of acid treatment in term of clinical
results compared with non-acid-treated controls
(36), both as to studies in combination with bone
grafting or guided tissue regeneration (96).In a study
by Fuentes et al. (36), a total of 27 mandibular degree
I1 furcation defects were treated using a coronally
positioned flap procedure with or without citric acid
conditioning of the root surfaces (Table 1).No statistically significant difference was found between acid
treated and non-acid-treated defects, indicating that

citric acid conditioning may not be a necessary part

of the regenerative coronally positioned flap procedure in mandibular furcations.

120

Bone grafting
The placement of bone grafts or alloplastic materials
in furcation defects in association with flap surgery
was evaluated in a large number of clinical trials and
animal experiments.
Biological concept
The biological rational behind the use of bone grafts
or alloplastic materials is the assumption that the
material may either 1) contain bone forming cells
(osteogenesis), 2) serve as a scaffold for bone formation (osteoconduction) or that 3) the matrix of the
grafting material contains bone inductive substances
(osteoinduction), which would stimulate both the
regrowth of alveolar bone and the formation of new

Regenerative therapy: furcation defects

tion. The use of autogenous cancellous bone from

extraction sites (Fig. 2) resulted in complete closure
of the approximal one third of the treated defects
with the formation of new cementum with inserting
collagen fibers (32). It was also reported that, during
healing of furcation defects, the fate of vital and nonvital autogenous transplants of mature cancellous
jaw bone was identical (33) and that xenografts (Fig.
3) such as Kielbone@(defattet and deproteinized ox
bone) displayed similar histological features as that
of fresh autogenous bone grafts during healing of
furcation defects (77).Nilvbus et al. (781, on the other
hand, failed to observe any favorable effect on healing of experimental furcation defects in dogs following the use of autogenous cancellous bone grafts
from extraction sites.
Clinical results

Fig. 6. Microphotograph of a titanium implant placed

without contact with retained roots (control). This implant has healed with a direct contact between the bone
and the implant surface (osseointegration).

attachment (11, 56). Such complete regeneration of

the periodontal attachment apparatus following
grafting procedures would imply that cells derived
from bone would possess the ability to form new cementum with inserting collagen fibers on a previously periodontitis-affected root surface. This assumption, however, is in conflict with the present
knowledge about the biology of periodontal wound
healing, that repopulation of the detached root surface with cells from the periodontal ligament is the
prerequisite for new attachment formation (13, 14,
107).

Animal experiments
The effect of various bone grafts and alloplastic materials was evaluated in furcation defects in experimental animals. Ellegaard et al. (32, 33) examined
the effect of bone grafting in experimental through
and through furcation defects in monkeys. A markedly higher frequency of furcation closure occurred
with bone grafts as compared with non-grafted sites,
particularly with the use of fresh autogenous hip
marrow grafts (Fig. 1). However, the use of this type
of graft often resulted in ankylosis and root resorp-

The use of bone grafts to promote periodontal regeneration in intraosseous or furcation defects was
evaluated in controlled clinical trials and in several
case reports. Histological evidence of periodontal regeneration in human intraosseous defects following
the use of autogenous or allogenic bone grafts has
been reported (9, 10, 30, 48, 99). Encouraging case
reports showing reduced probing depth and bone fill
of degree I1 furcation defects following transplantation of iliac grafts were presented by Schallhorn
(95). However, despite the apparent potential for
bone fill and histological studies suggesting periodontal regeneration, iliac grafts obtained limited
clinical use, probably because of the morbidity associated with the second surgery to obtain the graft
material and a certain risk of inducing root resorption (31). Most likely encouraged by the promising
results of the iliac grafts and in order to avoid the
drawbacks of the extraoral autogenous bone grafts,
allografts such as mineralized freeze-dried bone and
demineralized freeze-dried bone allografts received
great attention.
The effect of demineralized freeze-dried bone
allografts was evaluated in mandibular degree I1 and
I11 furcation defects in humans in combination with
citric acid root conditioning and coronal flap positioning (Table 1).Treatment with citric acid and coronal flap positioning with and without demineralized freeze-dried bone allografts resulted in similar
clinical improvements indicating no beneficial effect
of bone grafting. About 40% of the treated defects
became completely closed, irrespective of the use of
bone grafts (37). Similar results were reported by
Garrett et al. (40), who compared the use of coronal

121

7
7

15
15

composite synthetic graft

debridement

composite synthetic graft

autogenous graft

Pepelassi et al. (84)

Yukna et al. (111)

23

13

degree I1 furcation
mandibular

degree 111 furcation

mandibular

degree 11 furcation

mandibular

mandibular

degree I1 furcation
mandibular

15

Type

n
14
16

porous hydroxyapatite

+ demineralized

+ demineralized

citric acid

freeze-dried bone dografts

dura mater membrane + citric acid

Treatment

Kenney et al. (57)

Study

Defect

1.6
1.7

0.5

0.8
1.o

2.6

2.0
-0.3

2.2

2.4

Vertical
2.4

2.2

Horizontal

1.9
0.8

3.3
-0.2

1.6
-0.3

1.8

Horizontal
2.6
3.0

Defect fill (mm)

-0.4

1.8

Vertical
1.6
1.5

Clinical attachment
level change (mm)

1115
0115

017

017

21123

3/15

Closures
61 14
7116

Table 1. Controlled human clinical studies on furcations treated with citric acid, bone grafts, alloplastic materials or combined regenerative techniques

Regenerative therapy: furcation defects

flap positioning and dura mater membranes in degree I1 furcations which, in addition, were treated
with citric acid and demineralized freeze-dried bone
allografts. The results, however, obtained with coronal flap positioning were superior to those obtained following the use of dura mater membranes.
The results of treating degree I11 furcations with citric acid and coronal flap positioning with and without the placement of demineralized freeze-dried
bone allografts were much less promising than those
obtained in degree I1 furcations (38). Only 4 out of 27
defects were not diagnosed as through and through
defects following treatment.
A few human studies were published using alloplastic materials in association with the treatment of
furcation defects (Table 1). In a comparison of porous hydroxyapatite in the treatment of mandibular
degree I1 furcations with that of debrided control
treatment, significant improvements in attachment
level and bone fill were observed (57). Other studies
evaluating the effect of alloplastic and synthetic graft
materials in the treatment of furcation defects demonstrated clinical improvements beyond that obtained by debridement alone, or similar clinical
changes as that observed following the use of conventional bone graft materials (84, 111). However,
histological evidence that the use of alloplastic or
synthethic graft materials may lead to periodontal
regeneration has not yet been presented.

Guided tissue regeneration

Clinical application of guided tissue regeneration in
periodontal therapy involves the placement of a
physical barrier to ensure that the previously periodontitis affected root surface becomes repopulated
with cells from the periodontal ligament. During recent decades, guided tissue regeneration has been
applied in a number of clinical trials for the treatment of various periodontal lesions such as intrabony defects, degree I1 and degree I11 furcation involvements and recession defects (56).
Biological concept
The biologically based concept of guided tissue regeneration has evolved through a number of animal
experiments documenting that the progenitor cells
for the formation of a new connective tissue attachment to the root surface are residing in the periodontal ligament. A study in monkeys, in which both
gingival connective tissue and gingival epithelium

Fig. 7. Microphotograph of a mesiodistal histological section through a mandibular degree I1 furcation defect
treated 3 months previously with guided tissue regeneration (43). The entire root surface in the furcation is covered with a layer of newly formed cementum (arrows).

were prevented from contacting the root surface

during healing by the use of a barrier membrane,
suggested that this technique could ensure repopulation of the detached root surface with periodontal
ligament cells, thereby predictably producing a new
connective tissue attachment (42).
Animal experiments
The effect of placing nonbioresorbable or bioresorbable membranes on degree I1 and I11 furcation defects
as compared with that in control defects treated without membranes was evaluated in dogs (21,76, 16,88,
63). In both degree I1 and I11 furcation defects, guided
tissue regeneration treatment resulted in significantly
more gain of connective tissue attachment and regrowth of alveolar bone than control therapy.
In studies of Pontoriero et al. (88) and Lindhe et
al. (63), complete closure of through and through
furcation defects with the formation of a periodontal
ligament and regrowth of the alveolar bone was
achieved. It was suggested that the size of the furcation defects as well as the shape of the surrounding alveolar bone was determining for the outcome

123

expanded polytetrafluoroethylene
debridement

expanded polytetrafluoroethylene
debridement
__
connective tissue membrane
debridement

expanded polytetrafluoroethylene
debridement
collagen
debridement

collagen
debridement

polyglactin
debridement

expanded polytetrafluoroethylene
debridement

expanded polytetrafluoroethylene
debridement

collagen
debridement

expanded polytetrafluoroethylene
debridement

expanded polytetrafluoroethylene
debridement

Pontoriero et al. (87)

Caffesse et al. (17)

Mezler et al. (74)

Van Swol et al. (104)

Caton et al. (19)

Mellonig et al. (73)

Mellonig al. (73)

Wang et al. (106)

Ponteriero & Lindhe (89)

Pontoriero & Lindhe (89)

Paul et al. (83)

Lekovic et al. (62)

expanded polytetrafluoroethylene
debridement

Lekovic et al. (60)

Study
~
_ _ ~ _ _ _ _ Treatment
_ _ _
~ _ _ _ ~ _ _ _
Pontoriero et al. (86)
expanded polytetrafluoroethylene
debridement
~

18
18

10
10

8
8
12
12

11
11

20
20

28
10

17
17
7
7

15
15

9
4

21
21

12
12

21
21

1.6
1.1

degree I1 furcation
mandibular

degree I1 furcation
mandibular
maxillary interproximal

degree I1 furcation
maxillarybuccal

0.7
0.2

1.5
0.1

1.3
0.4

3.7
0.9

degree I1 furcation
mandibular
maxillary buccal

degree I1 furcation
maxillarv
degree I1 furcation
mandibular

1.4
1.7

1.0
0.2
1.6
1.0

2.4
-0.7

1.8
0.6

2.9
-0.1

degree I1 furcation
mandibular

degree I1 furcation
maxillary
degree I1 furcation
mandibular

degree I1 furcation
mandibular
__ _ _
degree I1 furcation
mandibular

degree 111 furcation

mandibular

degree I1 furcation
mandibular

Defect

1.7
0.7

2.2
0.1

0.8
0.3

2.9
1.0

Clinical attachment level

change (mm)
Vertical
Horizontal
Type
~ _ _ _ _ _ _
__
degree I1 furcation
3.5
3.7
mandibular
1.1
2.1

0.2

0.3

1.1
0.3

2.0
1.1

1.o
0.3

1.8
0.9
2.9
1.5

4.5
1.3

2.3
0.7

0.9
0.3
0.9
0.0

1.6
-0.2

~-

0.2
-0.1

2.4
0.9

1.7
0.7

1.5
0.6
0.7
0.4

2.0
-1.3

0.2
-0.2

Horizontal

Defect fill (mm)

Vertical

~-

1/18
0118

2/10
1/10

1111

15/20
5/20

8/21
0121

14/21
2121

Closures
-~

Table 2. Controlled human clinical studies comparing the results of guided tissue regeneration with those of flap surgery and debridement in
furcation defects

Regenerative therapy: furcation defects

Fig. 8. A. Mandibular first molar presenting with a buccal

degree I1 furcation. Note the presence of a wide zone of
keratinized gingiva and the position of the gingival margin at the cementoenamel junction. B. Furcation following flap elevation and defect debridement. The furcation
entrance has small dimensions in width and height. The
horizontal bone loss was 5 mm. Note the high mesial and
distal peaks of bone. C. An expanded polytetrafluoroethylene membrane positioned and sutured to fully cover the

furcation area. The collar of the membrane is located at the

cementoenaml junction. D. The buccal flap is coronally positioned to cover the barrier membrane completely. E. Removal of the barrier membrane after 5 weeks. Newly
formed tissue fill the furcation completely and cover most
of the buccal aspect of the roots. The tissue was firmly attached to the root surfaces. F. At 1 year, the furcation was
closed and the gingival margin was positioned at almost
the same level as prior to treatment.

of guided tissue regeneration treatment. The treatment failures were consistently associated with recession of the covering tissue flaps, which resulted
in exposure of the furcation defect. Provided this was
prevented, even comparatively large furcation de-

fects were successfully regenerated by guided tissue

regeneration therapy. The results also demonstrated
that bioresorbable membranes provided a barrier
that was equally effective to that of nonbioresorbable Teflon membranes (63).

125

Karring & Cortellini

Fig. 9. A. Mandibular first molar presenting with a 7-mmdeep buccal degree I1 furcation involvement. B. Furcation
following flap elevation. The furcation entrance is very
narrow and its height about 4 mm. Horizontal bone loss
amounted to 7 mm. Note the high mesial and distal bone
peaks. C. A nonbioresorbable barrier membrane is positioned and sutured with its border coronal to the ce-

mentoenamel junction. D. After membrane removal at 5

weeks, the furcation is filled with newly formed tissue.
E.The treated furcation after 1 year. The residual horizontal probing depth of the furcation is less than 1 mm. F. Reentry of the furcation after 1 year. The furcation is almost
completely filled with bone.

Clinical results

ports have addressed the predictability of guided

tissue regeneration treatment of mandibular or
maxillary degree I1 and I11 furcation defects. The results of studies evaluating the effect of guided tissue
regeneration treatment of furcation defects compared with that of debridement and flap surgery are

Histological evidence of new attachment in humans

(Fig. 7) has been presented following treatment of
various types of periodontal lesions with barrier
membranes (24, 43, 81). Studies and many case re-

126

Regenerative therapy: furcation defects

summarized in Table 2 . Although a certain variability

occurs in the clinical outcomes, the use of barrier
membranes generally demonstrates significant clinical advantages compared to debridement in mandibular degree I1 furcation defects. The reported average gains of vertical and horizontal clinical attachment in degree I1 defects treated with guided tissue
regeneration ranged from 0.7 to 3.7 mm and from 0.8
to 3.7 mm, respectively (Fig. 8). The corresponding
parameters for the control defects ranged from -0.7
to 1.7 mm and from 0.1 to 2.1 mm. The variations in
vertical and horizontal bone fill are 0.2 to 2.9 mm
and 0.2 to 4.5 mm for furcations treated wtih guided
tissue regeneration and -1.3 to 1.5 mm and -0.2 to
1.3 mm for the controls (Fig. 9). The most substantial
clinical improvement following guided tissue regeneration treatment of degree I1 mandibular furcations was reported by Pontoriero et al. (86), who
found complete closure of the furcation in 67% of
the test sites and in only 10% of the control sites.
Other studies, however, have failed to confirm these
promising results (Fig. 10). Very few studies report
about complete closure of furcation defects, and Van
Swol et al. (104), for instance, found no significant
difference in vertical clinical attachment level between membrane-treated and non-membranetreated degree I1 furcation defects The results of reentry measurements in this study, on the other hand,
indicated an advantage to the guided tissue regeneration treatment (Table 2). The observed differences in favor of guided tissue regeneration when
compared with debridement in the treatment of
mandibular degree I1 furcation defects are supported
by the results of a meta-analysis showing that compared to flap debridement, guided tissue regeneration results in greater reduction in probing depths
and greater gains in vertical and horizontal attachment (69).
Similar mean gains of clinical attachment (horizontal clinical attachment level from 2.3 to 3.3 mm)
in mandibular degree I1 furcations as that reported
in the controlled studies mentioned above (Table 2)
have been demonstrated in a number of case series
following the use of bioresorbable or nonbioresorbable barrier membranes (3, 59, 67, 68, 85). A comparative study of Anderson et al. (2), however, demonstrated that the gain of clinical attachment observed following treatment of mandibular degree I1
furcations with expanded polytetrafluoroethylene
barrier membranes was small (0.7 mm) and similar
to that obtained with coronal positioned flaps and
citric acid conditioning.
Significant improvement beyond debridement

was also observed in degree I1 buccal maxillary furcation defects following guided tissue regeneration
(89) but not to the same extent as in mandibular defects. Other investigators have failed to observe any
significant differences between debridement and the
use of guided tissue regeneration in maxillary molars
(73, 741, although these results were in the favour of
guided tissue regeneration treatment. Similarly, no
significant difference was noted between debridement and guided tissue regeneration treatment of
interproximal degree I1 defects in maxillary molars
(89).
Clinical improvement in mandibular degree 111
furcations following guided tissue regeneration has
been reported in a few studies. In a controlled study
by Pontoriero et al. (87), it was demonstrated that 8
out of 21 degree I11 mandibular furcations treated
with expanded polytetrafluoroethylene barrier membranes healed with complete closure of the defect,
while in the control group, none of the defects
healed completely (Table 2). Similar results were reported by Cortellini et al. (23) in a case series of 15
degree 111 mandibular furcations treated with barrier
membranes: 33% of these defects healed completely,
33% were partially healed and 33% were still through
and through following treatment (Fig. 11). A study
evaluating the use of expanded polytetrafluoroethylene barrier membranes on mandibular degree I11
furcations which, in addition, were treated with citric
acid, demineralized freeze-dried bone allografts and
coronal flap positioning also demonstrated limited
success (41).The majority of the treated defects were
still through and through at re-entry after 1 year, and
the use of a expanded polytetrafluoroethylene barrier membrane did not improve the results. Other
investigators have failed to observe complete closure
of any treated degree 111 furcations in mandibular or
maxillary molars following guided tissue regeneration treatment (3, 90). These reports indicate that
closure of mandibular class 111 furcations can be accomplished occasionally with guided tissue regeneration, but the result is unpredictable.
Clinical results of using bioresorbable collagen
and polymer barrier materials for the treatment of
bifurcation defects have been presented by several
investigators (Fig. 12, 13).The results of comparative
studies between treatment of degree I1 mandibular
furcation defects with nonbioresorbable and bioresorbable materials are summarized in Table 3. Little
clinical differences are noted between the groups.
The mean gain in vertical and horizontal clinical
attachment for furcations treated with nonbioresorbable barriers ranged from 0.0 to 1.3 mm and

127

Karring & Cortellini

128

Regenerative therapy: furcation defects

from 0.8 to 1.8 mm, respectively as compared with

0.0 to 1.8 mm and 1.5 to 2.5 mm for defects treated
with bioresorbable barrier membranes. The ranges
in vertical and horizontal bone fill are 0.4 to 1.0 mm
and 1.0 to 2.2 mm for nonbioresorbable membranes
versus 0.8 to 1.6 mm and 1.5 to 2.5 mm for defects
treated with bioresorbable materials. Bouchard et al.
(7), in particular, reported significantly greater horizontal clinical attachment level gain in the nonbioresorbable group compared with the bioresorbable
group, while Hugoson et al. (49) found the opposite.
The results indicate that generally there are no significant differences in clinical improvement between
bioresorbable or nonbioresorbable barrier materials
used to treat degree I1 furcation defects.
The results of comparative studies between
guided tissue regeneration treatment of furcation
defects with or without the adjunctive use of other
regenerative techniques are summarized in Table 4.
The average gains of vertical clinical attachment in
defects treated with guided tissue regeneration alone
ranged from -0.2 to 2.4 mm, compared to 0.8 to 4.3
mm for the combined treatment. The ranges in vertical and horizontal bone fill are 0.1 to 3.8 mm and
0.1 to 3.1 mm, respectively for guided tissue regeneration alone versus 2.3 to 5.1 mm and 1.6 to 4.2
mm for the combined treatment. A statistically significant improvement in terms of bone fill was demonstrated by Anderegg et al. (1) in the groups of furcations treated with combined therapy. A similar but
not statistically significant improvement of bone fill
in the furcation defect was reported by Lekovic et al.
(61), while Wallace et al. (105) failed to observe any
advantage of combined therapy. The results indicate
that an added benefit may be obtained by the use of
grafting materials in combination with barrier mem-

Fig. 10. A. Mandibular first molar presenting with a deep

buccal degree I1 furcation involvement. Note the recession
of the gingival margin. The furcation entrance is exposed.
B. The furcation after flap elevation and debridement.The
entrance of the furcation is large. Horizontal bone loss
was about 7 mm. C. A nonbioresorbable expanded polytetrafluoroethylene membrane is positioned and sutured
with its border coronal to the cementoenamel junction.
D. The buccal flap is coronally positioned to cover the
membrane. E. After 5 weeks, the membrane is still completely covered with gingiva. F.After removal of the membrane, it can be seen that the newly formed tissue almost
completely fills out the furcation. 6.The buccal flap is
replaced and sutured to protect the regenerated tissue.
H. At 1 year, a residual horizontal probing depth of 3 mm
is measured. The degree I1 furcation involvement was
transformed into a degree I furcation.

branes for the treatment of mandibular degree I1 furcations. Root conditioning in combination with
guided tissue regeneration was evaluated by Mactei
et al. (67) and Parashis & Mitsis (82). Both investigations failed to show significant differences between sites treated with barrier membranes alone or
in combination with root conditioning.

Factors affecting clinical outcome

There is conclusive evidence that significant clinical
improvement beyond that achieved with debridement alone can be obtained in mandibular degree I1
furcation defects following guided tissue regeneration treatment. However, the results are somewhat
variable, showing differences between the studies
and between individual experimental subjects. Using
multivariable approaches, a number of factors have
been identified that may be associated with the outcome of regenerative treatment of intrabony and furcation defects (68, 101, 102, 103). These are factors
related to 1) the patient, 2) the type of defect or 3)
the treatment technique.
Patient factors
The importance of proper plaque control on the outcome of regenerative therapy in intraosseous defects
is well established (25). Evidence that plaque control
and reinfection of the surgical site play a major role
in healing of mandibular degree I1 furcation defects
following guided tissue regeneration treatment was
provided by Machtei et al. (67, 68). Hugoson et al.
(49) also observed higher plaque scores in non-responding degree I1 furcations treated with guided
tissue regeneration as compared with those with a
successful outcome. A correlation between cigarette
smoking and poor outcomes of guided tissue regeneration therapy in mandibular degree I1 furcation
defects was reported (92). This finding is in agreement with results presented by Tonetti et al. (102)
showing less attachment level gains in intrabony defects following guided tissue regeneration therapy in
smokers than in nonsmokers.
Defect factors
It was shown that first and second mandibular molars and buccal and lingual degree I1 furcation defects respond equally well to guided tissue regeneration treatment (86, 68). However, in maxillary molars
the location of the furcation defect appears to play a

129

Karring & Cortellini

Fig. 11. A. A degree 111 furcation involved mandibular first

molar. B. After flap elevation and defect debridement, a
horizontal pattern of bone destruction is evident. The furcation entrance measured 5 mm in height and 3 mm in
width. A nonbioresorbable barrier membrane was placed
at both the buccal and the lingual furcation entrance.
C. At membrane removal after 6 weeks, the furcation is
incompletely filled with newly formed tissue. D. At 1 year,
a degree 111 furcation is still detectable. E. The 1-year reentry procedure showed some bone regrowth in the furcation area.

role, since no improvement beyond that of debridement was observed in interproximal degree I1 defects
compared to buccal defects (89). The furcation
lesion has the characteristics of a horizontal lesion,
which means that new attachment formation is dependent solely on coronal growth of periodontal
ligament tissue. This, in combination with the fact
that the anatomy of the furcation with its complex
morphology may prevent proper instrumentation
and debridement, makes healing of furcation defects
difficult. Studies in dogs have suggested that the size,
and especially the vertical height of furcation defects
plays a major role for a positive outcome of the

130

treatment (88). This corroborates observations in

humans that closure of degree I11 furcation defects
following guided tissue regeneration- treatment is
more likely to occur if the furcation do not exceed 3
mm in height (87). It was also demonstrated that the
initial defect depth is directly correlated with the
amount of attachment gain and bone formation in
mandibular degree I1 furcation defects treated with
guided tissue regeneration (67, 68). The deeper the
initial defect, the greater was the gain of horizontal
attachment and bone. Machtei et al. (681, however,
failed to demonstrate any relationship between the
morphology of the defects in terms of height, width,

Regenerative therapy:furcation defects

Fig. 12. A. Mandibular second molar. A buccal degree I1

furcation 6 mm deep was detected. There is some recession of the gingival margin, and the furcation entrance
is visible. B. After flap elevation it can be seen that the

furcation is large and measures about 4 mm in height.

C. A bioresorbable barrier membrane (Polylactide polymer) is used to cover the furcation entrance. D. At 1 year,
the residual horizontal probing depth is 2 mm.

depth and volume, and the outcome of guided tissue

regeneration treatment of mandibular degree I1 defects. Based on present evidence, successful outcome of guided tissue regeneration treatment can be
expected only in mandibular and in maxillary buccal
degree I1 furcations.

the coronal part of the material. Frequently, the margin of the gingival tissues recedes during the healing
period, thereby allowing further contamination of the
barrier material. The significance of the bacterial contamination was addressed in an investigation in surgically created furcation defects in monkeys (94). The
findings of this study showed that new attachment
and bone formation were favored considerably if bacteria were prevented from invading the membrane
and the wound during healing.
The effect of adjunctive antibiotic therapy in
guided tissue regeneration treatment of furcation
defects was evaluated by Demolon et al. (27, 28). The
clinical outcome of amoxicillin and clavulanate administration for 10 days in patients with mandibular
degree I1 defects treated with expanded polytetrafluoroethylene membranes were compared with
those in patients treated with membranes alone. Although the clinical signs of inflammation were significantly greater in patients treated with membranes alone during the first 14 weeks, no differ-

Technical factors
It is generally accepted that periodontal regeneration
is a technique-sensitive procedure requiring training
and experience. A flap management technique, which
positions the wound margin away from the entrance
to the healing defects, is essential for a positive outcome of regenerative treatment of furcation defects
(2,36,37).Another major determinant factor for successful regenerative therapy is postoperative infection
control. Bacterial contamination of the surgical site
may occur during surgery but also during the postoperative healing phase. After placement of a barrier
membrane, bacteria from the oral cavity may colonize

131

Karring & Cortellini

Fig. 13.A. Mandibular first molar presenting with a lingual

degree I1 furcation 6 mm deep. The gingival margin is
located coronally to the cementoenamel junction. B.After
flap elevation, it can be seen that the furcation entrance
is very large. C. A bioresorbable barrier membrane (Polylactide polymer) is positioned with its border coronal to
the cementoenamel junction to cover the furcation.
D. The lingual flap is sutured to cover the barrier membrane completely. E. The residual horizontal probing
depth at 1 year is 1 mm.

ences were found in clinical attachment gain

between the sites after 1 year. The authors suggested
that the use of antibiotics in conjunction with barrier
membranes may have controlled only the initial infection. Machtei et al. (67) investigated the effect of
adjunctive local application of antibiotics on treatment success of mandibular class I1 furcation defects
with expanded polytetrafluoroethylene membranes.
Prior to membrane placement, mechanically debrided furcations were irrigated with tetracycline,
whereas the contralateral sites were rinsed with saline. In addition, all patients received systemic tetracycline and rinsed with chlorhexidine postopera-

132

tively. At 12 months, similar improvement in horizontal and vertical clinical attachment level gains
were observed in both groups, regardless of tetracycline irrigation. Dowel1 et al. (29) also failed to observe any favorable effect on periodontal regeneration in degree I1 furcation defects by incorporating
metronidazole in collagen membranes as compared
with defects treated without antibiotic impregnated
membranes. Although data from controlled clinical
studies have failed to demonstrate a beneficial effect
of adjunctive local or systemic antibiotics on improvement of periodontal regeneration following
treatment of furcation defects with guided tissue re-

cu
cu

Treatment

Defect
n
Twe

Clinical attachment level

change (mm)
Vertical
Horizontal
1.0
1.0

1.0
2.0

Defect fill (mm)

Vertical
Horizontal

Closures

Wallace et al. (105)

Parashis & Mitsis (82)

Anderegg et al. (1)

Lekovic et al. (61)

Study

16

7
10

9
9

15
15

15
15

-dried 46

expanded polytetrafluoroethylene
expanded polytetrafluoroethylene + porous hydroxyapatite
expanded polytetrafluoroethylene
expanded polytetrafluoroethylene + demineralized freeze-dried
bone allografts
expanded polytetrafluoroethylene
expanded polytetrafluoroethylene + tetracycline
expanded polytetrafluoroethylene
expanded polytetrafluoroethylene + demineralized freeze-dried
bone alloerafts

Treatment

degree I1 furcation
mandibular
degree I1 furcation (27)
degree I11 furcation (3)
mandibular
degree I1 furcation
mandibular
degree I1 furcation
mandibular

Defect
n Type

0.8

-- 0.2

1.7
1.6

1.4
3.1

2.4
2.9

4.3

4.7
4.8

Clinical attachment
level change (mm)
Vertical Horizontal

3.8
5.0

1.7
3.5

0.1
2.3

2.3
2.4

1.0
2.4

0.1
1.6

Defect fill (mm)

Vertical Horizontal

217
3/10

(degree 11)

4/27

Closures

Table 4. Controlled human clinical studies comparing the results of guided tissue regeneration with or without the adjunctive use of other regenerative techniques in the treatment of furcation defects

Studv

Table 3. Controlled human clinical studies comparing the results of guided tissue regeneration with bioresorbable and nonbioresorbable membranes in the treatment of furcation defects

Karring & Cortellini

generation, further investigation should be carried

out to explore the possibility to improve the predictability of guided tissue regeneration treatment by
anti-infective therapy.

for at least 4 years, provided good oral hygiene and

frequent recall visits are established.

Conclusion
Long-term evaluation
A few studies have evaluated the long-term prognosis for furcation defects treated with regenerative
therapy. Sixteen mandibular degree I1 furcation defects, which originally following coronal flap positioning and citric acid root conditioning with and
without implantation of demineralized freeze-dried
bone allografts were determined as completely resolved with bone fill as assessed by re-entry surgery,
were re-evaluated after 4-5 years (47). Twelve of the
16 sites exhibited recurrent degree I1 furcations, and
all 16 sites demonstrated probable buccal furcation
defects. The investigators concluded that these findings question the long-term stability of bone regeneration in furcations following coronally advanced flap procedures.
The long-term stability of mandibular furcation
defects following guided tissue regeneration alone or
in combination with root conditioning and bone
grafting has also been reported (71). Of the 57% of
the furcation defects that were evaluated as completely filled at 6 and 12 months, only 29% were
completely filled after 4 to 6 years. However, 74% of
the furcations treated with guided tissue regeneration in combination with the placement of demineralized freeze-dried bone allografts were completely
filled at both the short- and long-term evaluation,
suggesting that the results obtained with the combined procedure were more stable over time. Longterm results of guided tissue regeneration treatment
of mandibular degree I1 furcations with expanded
polytetrafluoroethylene membranes were also reported by Machtei et al. (70). The teeth were followed up to 4 years and compared with non-furcated
molars. Improvements assessed in vertical and horizontal clinical attachment levels after treatment
were maintained also after 4 years, suggesting that
changes obtained in degree I1 furcation defects by
guided tissue regeneration are stable. Only 9% of the
treated defects were unstable which was similar to
that observed for non-furcated molars. Good oral
hygiene as reflected in low plaque scores and elimination of periodontal pathogens were closely related
to the long term stability. On the basis of these results, it was concluded that furcation defects treated
with membrane barriers can be maintained in health

134

Guided tissue regeneration represents the most welldocumented regenerative procedure for obtaining
periodontal regeneration in degree I1 furcation defects.
Guided tissue regeneration has demonstrated significant clinical improvements beyond that achieved
with debridement alone in treating degree I1 furcation defects. Regarding degree I1 maxillaiy furcations, the results are inconsistent, and the treatment of degree 111furcation defects is unpredictable.
An added benefit may be obtained by the use of
grafting materials in combination with guided tissue
regeneration for the treatment of mandibular degree
I1 furcations.
Differences in results between individuals and
studies in the treatment of class I1 furcation defects
is most likely related to patient compliance with
plaque control, maintenance procedures, selection
of defects, surgical management etc.
Periodontal regeneration obtained in degree I1
furcation defects following guided tissue regeneration is stable on a long-term basis, provided good
oral hygiene is maintained and a proper recall program is established.

References
1. Anderegg C, Martin S, Gray 1, Mellonig 1, Gher M. Clinical

2.

3.

4.

5.

evaluation of the use of decalcified freeze-dried bone allografts with guided tissue regeneration in the treatment
of molar furcation invasions. J Periodontol 1991: 62: 264268.
Anderson B, Bratthall G, Kullendorf B, Grondahl K,
Rohlin M, Attstrom R. Treatment of furcation defects.
Guided tissue regeneration versus coronally positioned
flap in mandibular molars; a pilot study. J Clin Periodontol 1994: 21: 211-216.
Becker W, Becker BE, Berg L, Pritchard I, Caffesse R, Rosenberg E. New attachment after treatment with root isolation procedures: report for treated class I11 and class I1
furcations and vertical osseous defects. Int J Periodontics
Restorative Dent 1988: 8 : 2-16.
Black S, Gher M, Sandifer J, Fucini S, Richardson C. Comparative study of collagen and expanded polytetrafluorethylene membranes in the treatment of human class I1
furcation defects. J Periodontol 1994: 65: 598-804.
Blumenthal NM. A clinical comparison of collagen membranes with e-PTFE membranes in the treatment of human mandibular class II furcation defects. J Periodontol
1993: 64: 925-933.

Regen ern title ~ l i e ~ i pfiji~rcutior

:
r defects
6. Bogle G, Adams D, Crigger M, Klinge B, Egelberg J. New
attachment after surgical treatment and acid conditioning of roots in naturally occurring periodontal disease in
dogs. J Periodont Res 1981: 16: 130-133.
7. Bouchard I: Ouhayoun 7, NilvCus R. Expanded polytetraflourethylene membranes and connective tissue grafts
support bone regeneration for closing mandibular class I1
furcations. J Periodontol 1993: 64: 1193-1198.
8. Bower R. Furcation morphology relative to periodontal
treatment. Furcation root surface anatomy. J Periodontol
1979: 50: 366-374.
9. Bowers GM, Chadroff B, Carnevale R, Mellonig J, Corio R,
Emerson J, Stevens M, Romberg E. Histologic evaluation
of new attachment apparatus formation in humans. Part
11. J Periodontol 1989: 60: 675-682.
10. Bowers GM, Chadroff B, Carnevale R, Mellonig J, Corio R,
Emerson J, Stevens M, Romberg E. Histologic evaluation
of a new attachment apparatus formation in humans.
Part 111. J Periodontol 1989: 60: 683-693.
11. Brunsvold MA, Mellonig J. Bone grafts and periodontal
regeneration. Periodonto12000 1993: 1: 80-91.
12. Buhler H. Evaluation of root-resected teeth. Results after
10 years. J Periodontol 1988: 59: 805-810.
13. Buser D, Warrer K, Karring T. Formation of a periodontal
ligament around titanium implants. J Periodontol 1990:
61: 597-601.
14. Buser D, Warrer K, Karring T, Stich H. Titanium implants
with a true periodontal ligament. An alternative to osseointegrated implants. Int J Oral Maxillofac Implants 1990:
5: 113-116.
15. Caffesse RG, Holden MJ, Kon S, Nasjleti CE. The effect of
citric acid and fibronectin application on healing following
surgical treatment of naturally occurring periodontal disease in beagle dogs. J Clin Periodontoll985: 12: 578-590.
16. Caffesse RG, Dominguez LE, Nasjleti CA, Castelli WA,
Morrison EC, Smith BA. Furcation defects in dogs treated
by guided tissue regeneration (GTR). J Periodontol 1990:
61: 45-50.
17. Caffesse R, Smith B, Duff B, Morrison E, Merril D, Becker
W. Class I1 furcations treated by guided tissue regeneration in humans: case reports. J Periodontol 1990: 61: 510514.
18. Carnevale G, Pontoriero R, Lindhe J. Treatment of furcation involved teeth. In: Lindhe J, Karring T, Lang NI: ed.
Clinical periodontology and implant dentistry. Copenhagen: Munksgaard, 1997: 682-710.
19. Caton J, Greenstein G, Zappa U. Synthetic bioabsorbable
barrier for regeneration in human periodontal defects. J
Periodontol 1994: 65: 1037-1045.
20. Claffey N, Bogle G, Bjorvatn K, Selvig KA, Egelberg J. Topical application of tetracycline in regenerative periodontal
surgery in beagles. Acta Odontol Scand 1987: 45: 141-146.
21. Claffey N, Motsinger S, Ambruster J, Egelberg J. Placement of a porous membrane underneath the mucoperiosteal flap and its effect on periodontal wound healing in
dogs. J Clin Periodontol 1989: 16: 12-16.
22. Cole RT, Crigger M, Bogle G, Egelberg J, Selvig KA. Connective tissue regeneration to periodontally diseased
teeth. A histological study J Periodont Res 1980: 15: 1-9.
23. Cortellini P, Pini-Prato G, Baldi C, Clauser C. Guided
tissue regeneration with different materials. Int J Periodontics Restorative Dent 1990: 10: 137-151.
24. Cortellini P, Clauser C, Pini Prato GI? Histologic assess-

ment of new attachment following the treatment of a human buccal recession by means of a guided tissue regeneration procedure. J Periodontol 1993: 64: 387-391.
25. Cortellini P, Pini Prato GP, Tonetti M. Periodontal regeneration of human intrabony defects. V. Effect of oral
hygiene on long term stability. J Clin Periodontol 1994:
21: 606-610.
26. Crigger M, Bogle G, Nilveus R, Egelberg J, Selvig KA. The
effect of topical citric acid application on the healing of
experimental furcation defects in dogs. J Periodont Res
1978: 13: 538-549.
27. Demolon IA, Persson GR, Johnson RH, Ammons WEEffect of antibiotic treatment of clinical conditions and bacterial growth with guided tissue regeneration. J Periodontol 1993: 64: 609-616.
28. Demolon LA, Persson GR, Ammons W, Johnson RH. Effect of antibiotic treatment on clinical conditions with
guided tissue regeneration: one year result. J Periodontol
1994: 65: 713-717.
29. Dowel1 I: A-Arrayed E Adam S, Moran J. A comparative
clinical study: the use of human type I collagen with and
without the addition of metronidazole in the GTR method
of treatment of periodontal tissue. J Clin Periodontol
1995: 22: 543-549.
30. Dragoo MR, Sullivan HC. A clinical and histological evaluation of autogenous iliac bone grafts in humans. I. Wound
healing 2 to 8 months. J Periodontol 1973: 44: 599-613.
31. Dragoo MR, Sullivan HC. A clinical and histological evaluation of autogenous iliac bone grafts in humans. 11. External root resorption. J Periodontol 1973: 44: 614-625.
32. Ellegaard B, Karring T, Listgarten M, Loe H. New attachment after treatment of interradicular lesions. J Periodontol 1973: 44: 209-217.
33. Ellegaard B, Karring T, Loe H. The fate of vital and devitalized bone grafts on the healing of interradicular lesion. J
Periodont Res 1975: 10: 88-97.
34. Erpenstein H. A three year study of hemisectioned molars. J Clin Periodontol 1983: 10: 1-10,
35. Frank RM, Fiore-Donno G, Cimasoni G. Cementogenesis
and soft tissue attachment after citric acid treatment in
human. An electron microscopic study. J Periodontol
1983: 54: 389-401.
36. Fuentes P, Garrett S, NilvCus R, Egelberg J. Treatment of
periodontal furcation defects. Coronally positioned flap
with or without citric acid root conditioning in class I1
defects. J Clin Periodontol 1993: 20: 425-430.
37. Gantes B, Martin M, Garrett S, Egelberg J. Treatment of
periodontal furcation defects. 11. Bone regeneration in
mandibular class I1 defects. J Clin Periodontol 1988: 15:
232-339.
38. Gantes B, Synowski BN, Garrett S, Egelberg J. Treatment
of periodontal furcation defects. Mandibular class 111 defects. J Periodontol 1991: 62: 361-365.
39. Garrett S, Crigger M, Egelberg J. Effects of citric acid on
diseased root surfaces. J Periodont Res 1978: 13: 155-163.
40. Garrett S, Martin M, Egelberg J. Treatment of periodontal
furcation defects. Coronally positioned flaps versus dura
mater membranes in class I1 defects. J Clin Periodontol
1990: 17: 179-185.
41. Garrett S, Gantes B, Zimmerman G, Egelberg J. Treatment
of mandibular class 111periodontal furcation defects. Coronally positioned flaps with and without e-PTFE membranes. J Periodontol 1994: 65: 592-597.

135

Karrint? & Cortellini

42. Gottlow J , Nyman S, Karring T, Lindhe J. New attachment
formation as the result of controlled tissue regeneration.
J Clin Periodontol 1984: 11: 494-503.
43. Gottlow J, Nyman S, Lindhe J, Karring T, Wennstrom J.
New attachment formation in the human periodontium
by guided tissue regeneration. J Clin Periodontol 1986: 13:
604-6 16.
44. Hamp SE, Nyman S, Lindhe J. Periodontal treatment of
multirooted teeth after 5 years. J Clin Periodontol 1975: 2:
126-1 35.
45. Hamp SE, Ravald N, Tewik A, Lundstrom A. Perspective a
long terme des modalitks de traitement des lesions interradiculairis. J Parodontol 1992: 11: 11-23.
46. Langer B, Stein SD, Wagenberg B. An evaluation of root
resections. A ten year study. J Periodontol 1981: 52: 719722.
47. Haney JM, Leknes KN, Wikesjo UME. Recurrence of mandibular molar furcation defects following citric acid root
treatment and coronally advanced flap procedures. Int J
Periodontics Restorative Dent 1997: 17: 3-10.
48. Hiatt WH, Schallhorn RG, Aaronian AJ, The induction of
new bone and cementum formation. n! Microscopic examination of the periodontium following human bone
and marrow allograft and non-graft periodontal regenerative procedures. J Periodontol 1978: 49: 495-512.
49. Hugoson A, Ravald N, Fornell J, Johard G, Teiwik A,
Gottlow J. Treatment of class I1 furcation involvements in
humans with bioresorbable and non-bioresorbable
guided tissue barriers. A randomized multicenter study. J
Periodontol 1995: 66: 624-634.
50. Isidor F, Karring T, Nyman S, Lindhe J. New attachment,
re-attachment following reconstructive periodontal
surgery. J Clin Periodontol 1985: 12: 728-735.
51. Kalkwarf KL, Kaldahl WB, Patil KD. Evaluation of furcation
region response to periodontal therapy. J Periodontol
1988: 59: 794-804.
52. Karring T, Nyman S, Lindhe J. Healing following implantation of periodontitis affected roots into bone tissue. J
Clin Periodontol 1980: 7: 96-105.
53. Karring T, Nyman S, Lindhe J, Sirirat M. Potentials for root
resorption during periodontal healing. J Clin Periodontol
1984: 11: 41-52.
54. Karring T, Isidor F, Nyman S, Lindhe J. New attachment
formation on teeth with a reduced but healthy periodontal ligament. J Clin Periodontol 1985: 12: 51-60.
55. Karring T, Nyman S, Gottlow J, Laurell L. Development of
the biological concept of guided tissue regeneration - animal and human studies. Periodontol2000 1993: 1: 26-35.
56. Karring T, Lindhe J, Cortellini ? Regenerative periodontal
therapy. In: Lindhe J, Karring T, Lang NF) ed. Clinical periodontology and implant dentistry. Copenhagen: Munksgaard, 1997: 597-646.
57. Kenney EB, Lekovic V, Elbaz JJ, Kovacric K, Carranza FA,
Takei HH. The use of a porous hydroxylapatite implant in
periodontal defects 11. Treatment of class 11 furcation
lesions in lower molars. J Periodontol 1988: 59: 67-72.
58. Klinge B, NilvCus R, Egelberg J. Effect of defect size and
flap placement on healing of experimental furcation defects in dogs. J Periodont Res 1981: 16: 236-248.
59. Laurell L, Falk H, Fornell J, Johard G, Gottlow J. Clinical
use of a bioresorbable matrix barrier in guided tissue regeneration therapy. Case series. J Periodontol 1994: 65:
967-975.

136

60. Lekovic V, Kenney E, Kovacevic K, Carranza F. Evaluation

of guided tissue regeneration in class I1 furcation defects.
A clinical re-entry study. J Periodontol 1989: 60: 694-698.
61. Lekovic V, Kenney EB, Carranza FA, Danilovic V. Treatment of class I1 furcation defects using porous hydroxylapatite in conjunction with a polytetrafluorethylene
membrane. J Periodontol 1990: 61: 575-578.
62. Lekovic V, Kenney EB, Carranza FA, Martignoni M. The
use of autogenous periosteal grafts as barriers for the
treatment of class I1 furcation involvements in lower molars. J Periodontol 1991: 61: 775-780.
63, Lindhe J, Pontoriero R, Berglundh T, Araujo M. The effect
of flap management and bioresorbable occlusive devices
in GTR treatment of degree 111 furcation defects. An experimental study in dogs. J Clin Periodontol 1995: 22:
276-283.
64. Listgarten MA, Rosenberg MM. Histological study of repair following new attachment procedures in human
periodontal lesions. J Periodontol 1979: 50: 333-344.
65. Listgarten MA. Periodontal probing: What does it mean?
J Clin Periodontol 1980: 7: 165-176.
66. Little LA, Beck FM, Bugci B, Horton JE. Lack of furcal bone
loss following the tunneling procedure. J Clin Periodontol
1995: 22: 637-641.
67. Machtei E, Dunford R, Norderyd J, Zambon J, Genco R.
Guided tissue regeneration and anti-infective therapy in
the treatment of class I1 furcation defects. J Periodontol
1993: 64: 968-973.
68. Machtei E, Cho M, Dunford R, Norderyd J, Zambon J,
Genco R. Clinical, microbiological and histological factors
which influence the success of regenerative periodontal
therapy. J Periodontol 1994: 65: 154-161.
69, Machtei E, Schallhorn RG. Successful regeneration of
mandibular class I1 furcation defects. An evidence-based
treatment approach. Int J Periodontics Restorative Dent
1995: 15: 146-167.
70. Machtei E, Grossi S, Dunford R, Zambon J, Genco R.
Long-term stability of class I1 furcation defects treated
with barrier membranes. J Periodontol 1996: 67: 523-527.
71. McClain E: Schallhorn RG. Long term assessment of combined osseous composite grafting, root conditioning and
guided tissue regeneration. Int J Periodontics Restorative
Dent 1993: 13: 9-27.
72. Melcher AH. On the repair potential of periodontal
tissues. J Periodontol 1976: 47: 256-260.
73. Mellonig 7, Semons B, Gray J, Towle H. Clinical evaluation
of guided tissue regeneration of grade I1 molar furcation
invasion. Int J Periodontics Restorative Dent 1994: 14:
255-271.
74. Metzler DG, Seamons BC, Mellonig JT, Gher ME, Gray JL.
Clinical evaluation of guided tissue regeneration in the
treatment of maxillary class I1 molar furcation invasions.
J Periodontol 1991: 62: 353-360.
75. Muller HE: Egert T, Lange DE. Management of furcationinvolved teeth. A retrospective analysis. J Clin Periodontol
1995: 22: 911-917.
76. Niederman R, Savitt ED, Heeley JD, Duckworth JE. Regeneration of furca bone using Gore-Tex Periodontal Material. Int J Periodontics Restorative Dent 1989: 9: 469-479.
77. Nielsen IM, Ellegaard B, Karring T. Kielbone@in healing
interradicular lesions in monkeys. J Periodont Res 1980:
15: 328-337.
78. Nilveus R, Johansson 0, Egelberg J. The effect of autogen-

Regenerative therapy: furcation defects

ous cancellous bone grafts on healing of experimental
furcation defects in dogs. J Periodont Res 1978: 13: 532537.
79. NilvCus R, Bogle G, Crigger M, Egelberg J, Selvig KA. The
effect of topical citric acid application on the healing of
experimental furcation defects in dogs. 11. Healing after
repeated surgery. J Periodont Res 1980: 15: 544-550.
80. Nyman S, Karring T, Lindhe J, PlantCn S. Healing following
implantation of periodontitis-affected roots into gingival
connective tissue. J Clin Periodontol 1980: 7: 394-401.
81. Nyman S, Lindhe J, Karring T, Rylander H. New attachment following surgical treatment of human periodontal
disease. J Clin Periodontal 1982: 9: 290-296.
82. Parashis A, Mitsis E Clinical evaluation of the effect of
tetracycline root preparation on guided tissue regeneration in the treatment of class I1 furcation defects. J Periodontol 1993: 64: 133-136.
83. Paul BE Mellonig JT, Towle HJ, Gray JL. The use of a collagen barrier to enhance healing in human periodontal furcation defects. Int J Periodontics Restorative Dent 1992:
12: 123-131.
84. Pepelassi, EM, Bissada NE Greenwell H, Farah CF. Doxycycline-tricalcium phosphate composite graft facilitates
osseous healing in advanced periodontal furcation defects. J Periodontol 1991: 62: 106-115.
85. Polson A, Garrett S, Stoller NH, Greenstein G, Polson AE:
Harrold CQ, Laster L. Guided tissue regeneration in human furcation defects after using a biodegradable barrier:
a multi-center feasibility study. J Periodontol 1995: 66:
377-385.
86. Pontoriero R, Lindhe J, Nyman S, Karring T, Rosenberg E,
Sanavi E Guided tissue regeneration in degree I1 furcation-involved mandibular molars. A clinical study. J
Clin Periodontol 1988: 15: 247-254.
87. Pontoriero R, Lindhe J, Nyman S, Karring T, Rosenberg E,
Sanavi E Guided tissue regeneration in the treatment of
furcation defects in mandibular molars. A clinical study
of degree I11 involvements. J Clin Periodontol 1989: 16:
170-174.
88. Pontoriero R, Nyman S, Ericsson I, Lindhe 7. Guided
tissue regeneration in surgically produced furcation defects. An experimental study in the beagle dog. J Clin Periodontol 1992: 19: 159-163.
89. Pontoriero R, Lindhe J. Guided tissue regeneration in the
treatment of degree I1 furcations in maxillary molars. J
Clin Periodontol 1995: 22: 756-763.
90. Pontoriero R, Lindhe J. Guided tissue regeneration in the
treatment of degree 111 furcations in maxillary molars.
Short communication. J Clin Periodontol 1995: 22: 810912.
91. Ririe CM, Crigger M, Selvig KA. Healing of periodontal
connective tissues following surgical wounding and application of citric acids in dogs. J Periodont Res 1980: 15:
314-327.
92. Rosenberg ES, Dent HD, Cutles SH. The effect of cigarette
smoking on the long-term success of guided tissue regeneration: a preliminary study. Ann R Aust Coll Dent
Surg 1994: 112: 89-93.
93. Ross IF, Thompson RH. Furcation involvement in maxillary and mandibular molars. J Periodontol 1980: 51: 450454.
94. Sander L, Karring T. New attachment and bone formation
in periodontal defects following treatment of submerged

roots with guided tissue regeneration. J Clin Periodontol

1995: 22: 295-299.
95. Schallhorn RG. Eradication of bifurcation defects utilizing
frozen autogenous hip marrow implants. Periodont Abstr
1967: 15: 101-105.
96. Schallhorn RG, McClain PK. Combined osseous composite
grafting, root conditioning and guided tissue regeneration.
Int J Periodontics Restorative Dent 1988: 4: 9-31.
97. Selvig KA, Ririe CM, Nilveus R, Egelberg J. Fine structure
of new connective tissue attachment in experimental furcation pockets in dogs. J Periodont Res 1981: 16: 123-129.
98. Stahl S, Slavkin HC, Yamada L, Levine S. Speculations
about gingival repair. J Periodontol 1972: 43: 395-402.
99. Stahl S, Froum S, Kushner L. Healing responses of human
teeth following the use of debridement grafting and citric
acid root conditioning. 11. Clinical and histologic observations: one year post- surgery. J Periodontol 1983: 54:
325-338.
100. Stahl S, Froum S. Healing of human suprabony lesions
treated with guided tissue regeneration and coronally anchored flaps. J Clin Periodontol 1991: 18: 69-74.
101. Tonetti M, Phi-Prato G, Cortellini ? Periodontal regeneration of human infrabony defects. IV. Determinants of the
healing response. J Periodontol 1993: 64: 934-940.
102. Tonetti M, Pini-Prato G, Cortellini I? Effect of cigarette
smoking on periodontal healing following GTR in
infrabony defects. A preliminary retrospective study J
Clin Periodontol 1995: 22: 229-234.
103. Tonetti M, Pini-Prato G, Cortellini I? Factors affecting the
healing response of intrabony defects following guided
tissue regeneration and access flap surgery. J Clin Periodontol 1996: 23: 548-556.
104. Van Swol R, Ellinger R, Pfeifer J, Barton N, Blumenthal N.
Collagen membrane barrier therapy to guide regeneration
in class I1 furcations in humans. J Periodontol 1993: 64:
622-629.
105. Wallace S, Gellin R, Miller C, Miskin D. Guided tissue regeneration with and without decalcified freeze-dried
bone in mandibular class I1 furcation invasions. J Periodontol 1994: 65: 244-254.
106. Wang H, ONeal R, Thomas C, Shyr Y, MacNeil R. Evaluation of an absorbable collagen membrane in treating
class I1 furcation defects. J Periodontol 1994: 65: 10291036.
107. Warrer K, Karring T, Godtfredsen K. Periodontal ligament
formation around different types of dental titanium implants. I. The selftapping screw type implant system. J
Periodontol 1993: 64: 29-34.
108. Wikesjo UME, Claffey N, Christersson LA, Genco RJ, Terranova W, Egelberg J. Repair of periodontal furcation defects in beagle dogs following reconstructive surgery including root surface demineralization with tetracycline,
hydrochloride and topical fibronectin application. J Clin
Periodontol 1988: 15: 73-80.
109. World Workshop in Periodontology 1996. Ann Periodontol
1996: 1: 618-870.
110. Yukna R. Clinical human comparison of expanded polytetrafluorethylene barrier membrane and freeze-dried dura
mater allografts for guided tissue regeneration of lost
periodontal support. J Periodontol 1992: 63: 421-442.
111. Yukna RA. Clinical evaluation of HTR polymer bone replacement grafts in human mandibular class I1 molar furcations. J Periodontol 1994: 65: 342-349.

137