Int. J. oral Surg. 1972: 1:148-160
(Key
words:
emlodontlc surgery; periapical healing)
Modes of healing histologically
after endodontic surgery in 70 cases
J. O. ANDREASEN AN'D JI3RGEN RUD
Detztal Department, University Hospital (Rigshospitalet),
Department of Oral Pathology, Royal Dental College, Copenhagen, Denmark
ABSTRACT- - The histologic changes in humans after endodontic surgery
were studied in 70 biopsies of the root apex and surrounding soft
tissues and bone obtained from less than one year to 1.4 years after
the surgical procedures. The following aspects were examined: degree
of inflammation, formation of new cementum, root resorption, regeneration of the periodontal ligaments, formation of fibrous scar tissue,
ankylosis, presence of granulation tissue and epithelial proliferations,
and regeneration of new bone. The histologic examination revealed
thaf the results of periapical surgery could be divided into three main
types: (1) healing with re-formation of the periodontal membrane or
ankylosis, and no or mild periapical inflammation, (2) healing with
fibrous tissue (scar tissue) in communication with or adjacent to the
periodontal membrane, occasional ankylosis, and varying grades of
inflammation, and (3) moderate or severe periapical inflammation
without scar tissue.
(Received for publication 21 August, accepted 2 September 1972)
The healing events taking place after periapical surgery include repair of all periodontal components: cementum, periodontal
ligaments and bone.
Our present histologic knowledge of the
capacity and mode of healing of the periodontium after endodontic surgery is rather
limited a n d is based on case reports which
deal m a i n l y with unsuccessful cases (Kronfeld 1928, Coolidge 1930, Hill 1931, Hiiupl
1932, Steinhardt 1933, Moen 1940, Herbert
1941, 1943, Sommer 1946, Weaver 1947,
Winkelmair 1948, Frankt 1948, Rowe 1967,
Smith 1967).
The present study has therefore used a
larger material, including both successful as
well as unsuccessful cases, to analyze the
histologic variations in healing of the periodontium after endodontic therapy.
MATERIAL AND METHODS
The material consisted of 70 biopsies including
the root apex and surrounding periapical tissues obtained in the follow-up period after
surgical treatment of periapical inflammatory
changes or cystic lesions.
Fifteen patients were operated at the Dental
Clinic at the University Hospital, Copenhagen,
mad 55 cases were operated and later biopsied
by one of the authors (J.R.) in a private practice limited to oral surgery.
HISTOLOGIC HEALING AFTER ENDODONTIC SURGERY
The majority of biopsies were from cases of
endodontic surgery which, after several years,
were suspected of not having healed properly.
The present material therefore represents selected cases, and the ratio between successful
and unsuccessful cases is not the same as would
be found in consecutively treated cases.
The clinical data for these operations, including the observation periods, are listed in Table
1.
The biopsy technique used was that described
by Nygaard-0stby (1948). With a thin surgical
bur a block was removed including the apex
and surrounding periapical soft tissues and
bone. The specimens were fixed in 10 go formalin and later demineralized in formic acid/
sodium citrate. If retrograde amalgam fillings
were present, these were removed after demineralization with a needle or a bur. The
specimens were embedded after double infiltration in ceIloidin-paraffin. Forty-seven specimens were cut in the mesio-distal direction
along the axis of the tooth, whereas the remaining cases were sectioned in a vestibulo-lingual
direction. Step serial sections were made in 43
149
cases (Stanley 1957); 27 specimens were sectioned completely. An average of 197 sections
were available from each biopsy. Every fifth
section was stained with hematoxylin-eosin and
used for evaluation.
Periapical inflammatory changes were graded
into the following four groups: I, none; 2,
mild; 3, moderate; 4, severe. Details of this
grading are given in a related article (Andreasen & Rud 1972).
RESULTS
The histological e v a l u a t i o n r e v e a l e d three
post-operative conditions of t h e periodontal
ligaments and supporting bone: (1) h e a l i n g
with re-formation of the periodontal m e m brane or ankylosis, and n o or m i l d periapica[
inflammation, (2) healing with fibrous tissue
(scar tissue) in c o m m u n i c a t i o n with o r adjacent to the periodontal ligament, occasional
ankylosis, and v a r y i n g grades of i n f l a m m a -
Table 1. Clinical data for 70 cases of endodontic surgery with histologic examination of root
apices, periapical structures ;rod surrounding bone
Sex of patients: 15 males, 55 females.
Age o/ patients at time of endodontic surgery
Years:
0-24
25-34
Number:
7
26
35-44
24
45-54
8
55-89
5
Type o/ teeth
Type:
Number:
1
9
2
31
Maxillary
3
4
6
3
5
7
6
0
1
2
8
3
Resection of root and type of root filling
Resection
Resection
Retrograde
Orthograde
Amalgam
Guttapercha
20
37
Mandibular
3
4
3
5
0
6
0
0
Apical curettage
Orthograde
Guttapercha
13
Type o/ periapical lesion
10 cysts, histologically verified at time of endodontic surgery, 60 granulomas
Stage of inflammation o/ peHapical lesion at time of operation
61 chronic
7 subacute
Time between endodontic surgery and biopsy
YeArs:
~1
1
2
3
4
Number:
3
18 13 11 3
5
4
6
7
7
5
8
2
2 acute
9
0
10
1
11
0
12
2
13
0
14
1
150
ANDREASEN AND RUD
Table 2. Histologic changes found in 70 cases after endodontic surgery
Healing
Healing
Periapical
with
with
inflamre-formation fibrous scar
marion
of a
tissue
without scar
periodontal
tissue
membrane
10 cases
35 cases
25 cases
Cementum repair
No repair
Partial repair
Complete repair
No root resection
Not evaluable
Root resorption and
cementum repair
Cementum formed without
previous resorption
Cementum formed after
previous resorption
Resorption arrested
Active resorption
Not evaluable
Ankylosis
0
I
5
3
1
7
13
6
9
4
15
4
0
1
5
8
1.0
4
0
1
0
4
15
8
0
9
5
0
1
Present
Not present
2
8
3
32
0
25
Bone marrow
Fat marrow
Fat and fibrous marrow
Fibrous marrow
Not evaluable
5
0
3
2
8
3
7
17
1
0
9
15
Epithelial
proliferation
Present
Not present
0
i0
5
30
14
II
Inflammation
No
2
8
0
0
4
14
10
7
0
0
4
21
Mild
Moderate
Severe
tion, and (3) moderate or severe periapical
i n f l a m m a t i o n without scar tissue.
T h e histologic findings within these three
healing groups are shown in Table 2. These
findings will be described further in the
following.
Healing with re-formation of periodontal
ligament
T e n teeth were examined histologically in
this group (Table 2). I n five cases the resected r o o t surface showed complete repair
with new cementum (Fig. 1). T h e thickness
of the new cementum was found to decrease
from the lateral to the central parts of the
resected root surface. T h e n ew cementum
was most often acellular. In f i v e cases the
cementum was formed without preceding
resorption of the root surface, whereas four
cases showed evidence in some areas of root
resorption before cementum repair. Only
one case showed active root resorption, i.e.
with uni- or multinuclear connective tissue
cells present adjacent to the resorption
HISTOLOGIC HEALING AFTER ENDODONTIC SURGERY
areas. N o cementum repair was found in
these areas.
In the lateral parts of the resected root
surface, collagen fibers were attached to the
new cementum and bone in a normal fiber
arrangement, while centrally these fibers
paralleled the root surface and formed a
fibrous capsule covering the root filling (Fig.
2). In two cases small areas of the periodontal ligament were replaced by a bony
union (ankylosis) between the root surface
and the surrounding bone (Fig. 3). The
periodontal tissue adjacent to the root filling
was free of inflammatory ceils in only two
cases (Fig. 3), while eight cases showed a
mild chronic infiltration with lymphocytes,
plasma cells and macrophages (Fig. 2). In
all ten cases the alveolar bone showed regeneration with a lamina dura (Figs. 1-3). In
three cases the bone marrow, corresponding
to the surgical defect, was replaced with
fibrous tissue (Fig. 2).
Healing with fibrous scar tissue
Thirty-five specimens demonstrated this type
of healing (Table 2). In 15 cases a defect in
the facial cortical bone plate was found
(Fig. 4). The scar tissue was characterized
by collagenous fibers running parallel to
the root surface and only few cellular components (Fig. 5). Where scar tissue was
found adjacent to the root surface, cementum repair was partial in 13 cases and missing in 7 cases. In 18 cases evidence of root
resorption was present before cementum
repair was found, whereas 8 cases showed
an active root resorption area. In 3 cases an
ankylosis was present (Fig. 6). The periodontal tissues adjacent to the root filling
were without inflammatory changes in 4
cases, whereas 14, ]0 and 7 cases showed
mild, moderate or severe inflammation,
respectively. In 5 cases proliferation of epithelium was found in the periapical soft tissues or partly covering the root surface. In
one case this epithelial lining was one to
151
two cell layers thick only, and no inflammatory changes were found in the adjacent
connective tissue (Fig. 7). I n 7 cases the
bone marrow peripheral to the scar tissue
was replaced with fibrous tissue (Fig. 7).
Moderate or severe periapicaI inflammation
Twenty-five specimens were examined in
this group: 4 cases with moderate and 21
cases with severe inflammation (Table 2).
While 4 cases showed formation of new
cementum, 16 roots showed only a partial
repair of cementum, and 4 roots showed no
cementum repair at all.
Signs of root resorption were found in 14
cases: 5 with arrested resorption and 9 roots
with evidence of previous resorption, before
cementum repair.
No instance of ankylosis was recorded
within this group. All cases showed granulation tissue adjacent to the root filling (Fig.
8). Signs of epithelium were found in 14 of
the 25 cases in the group: in 10 cases as
epithelial proliferations in the granulation
tissue, and in 4 cases as epithelial lined
cyst cavities.
In 9 cases the normal bone marrow was
replaced with fibrous tissue.
DISCUSSION
Newly formed cementum was observed to be
most abundant in the peripheral parts of the
resected root surface, suggesting that it
originated from the intact lateral parts of
the root. I n the present material it could not
be determined when the first cementum was
deposited, but in a histologic examination of
a human tooth extracted three weeks after
root resection, Hoenig (1935) found parts
of the resected root surface covered with
new cementum, and the same finding was
reported by Csernyei (1932) in experiments
on dogs.
As shown in the present study, initial
resorption of the root surface was appar-
152
A N D R E A S E N AND R U D
Fig. 1. Healing with re-formation of the periodontal ligament, and a mild periapical inflammation, A, condition of maxillary second premolar immediately after surgery. B, radiograph at follow-up 6 years later. C, low power view of surgical specimen. X 7. D, a mild inflammation is
found adjacent to the root filling. X 30. E, palatal part of the resected root surface covered
with new cementum. X 30. F, higher magnification of E. Note the normal structured periodontal ligament. X 30. G, normal bone marrow X 75.
.Fig. 2. Healing with re-formation of the periodontal membrane and fibrosis of bone marrow.
A, condition of mandibular right central incisor immediately after surgery. B, radiograph at follow-up l0 years later. C, low power view of surgical specimen. X 10. D, normal periodontal
ligament and cementum repair. X 30. E and F, mild inflammation in relation to the root filling
and collagen fibers running parallel to the root surface. M 30 and X 195. G, bone marrow
replaced with fibrous connective tissue. X 30.
H[STOLOGIC
HEALING
AFTER ENDODONTIC
SURGERY
153
154
ANDREASEN AND RUD
HISTOLOGIC HEALING AFTER ENDODONTIC SURGERY
155
Fig. 4. Healing with fibrous tissue of a maxillary right lateral incisor. A, radiographic examination 5 years after the operation. B, lateral view of surgical specimen. The facial bone plate is
missing over the resected part of the root. C, low power view of surgical specimen. Fibrous tissue covering the resected root surface. Labial bone plate is missing. X 7.
ently not necessary before new deposition of
cementum could take place. A remarkable
finding in this and in other studies was
that areas of the resected root surface were
sometimes found to be without cementum
repair even after long observation periods
(Aisenberg 1931, Blum 1932, Ltitgens 1938,
Brosch 1939, 1955, Droba 1942, Heiss
1942).
The rdgeneration of the periodontal ligaments usually consisted in the formation of
a fibrous capsule covering the root end; the
arrangement of the fibers seemed to preclude a normal supporting function of the
ligaments.
Formation of fibrous scar tissue in relation to the resected root surface was found
often. This type of periapical repair has
previously been examined histologically by
Jarzab (1930), H a m m e r (1933), Brosch
(1939, 1941) and Penich (1961). The etiology and pathogenesis of the development
of scar tissue within the jaw have been the
subject of a number of histologic studies.
Under experimental conditions in dogs,
Csernyei (1925, 1932, 1933, 1.935) found
that removal of a large portion of the :facial
bone plate is usually followed by incomplete
healing and formation of periapical scar
tissue. Similar findings in humans were reported by Boyne, Lyon & Miller (1961) a n d
Hj6rting-I-Iansen (1970). Another theory has
been that inflammatory changes or disturbed
function of the tooth m a y impede bone
healing, whereafter repair is accompanied b y
the formation of fibrous scar tissue (Broseh
1939).
Ankylosis between the r o o t surface a n d
the alveolar bone was found in five cases
(7 %), a finding not hitherto reported after
periapical surgery. Histologic studies after
conservative root filling therapy have shown
almost the same frequency of ankylosis
(Brynolf 1967, Seltzer, Soltanoff & Bender
1967).
The frequency of epithelial proliferation
in the periapical area was shown in this and
other studies (Brynolf 1967) to be related to
Fig. 3. Healing with ankylosis and no periapical inflammation. A, radiograph immediately after
surgery of maxillary right incisors. B, condition 8 years later. The apex of the central incisor
was removed. C, low power view of surgical specimen. X 10. D, cementum repair after initial
resorption. X 70. E and F, no inflammation in relation to the root filling. X 30 and X 70. G
and H, area with ankylosis. X 30.
156
ANDREASEN
AND
RUD
Fig, 5. H e a l i n g with fibrous tissue and n o inflammation. A, condition of maxillary left lateral
incisor immediately after surgery. B, radiograph taken 4 years later, C, low power view of surgical specimen. X 2tO. D, f~brous scar tissue. X 70. E, no inflammation in relation to root filling. X 30. F, thin layer of basophilic c e m e n t u m deposited on the resected root surface. X 70.
Fig. 6. H e a l i n g wittt fibrous tissue and ankylosis. A, condition immediately after removal of an
apical cyst a n d root filling of b o t h maxillary right incisors. B, radiograph taken 7 years later.
C, r a d i o g r a p h of surgical specimen. D, low power view of lateral incisor. T h e apex is surrounded by c o n n e c t i v e scar tissue. X 10. E, no inflammation in relation to the root filling. X 30. 1~',
no c e m e n t u m repair in relation to the fibrous tissue. X 70. G, bone deposited on mesial surface of the r o o t after resorption of cementum. X 30. H, new bone deposited on c e m e n t u m without previous resorption on distal root surface. X 30.
HISTOLOGIC
HEALING
AFTER E N D O D O N T I C
SURGERY
157
158
ANDREASEN AND RUD
Fig. 7. Healing with fibrous tissue and epitheIial cover on root surface. A, condition of maxillary left lateral incisor immediately after surgery. B, radiograph taken 2 years later. C, low
power view of surgical specimen. Scar tissue surrounds the apex. M 10. D, thin epithelium covering the root surface. No inflammation is seen in the adjacent fibrous tissue. M 195.
the extent o f inflammation. This finding
lends support to the hypothesis that the inf l a m m a t i o n m a y stimulate the proliferation
of epithelial remnants, such as cell rests of
Malassez or remaining cyst epithelium.
In a few cases epithelium was without inf l a m m a t o r y changes. A recent report, based
on histologic findings after conservative root
filling therapy, seems to indicate that such
epithelium m a y become stationary or eventual[y degenerate (Seltzer, Soltanoff & Bender 1969).
A c k n o w l e d g m e n t s - This study has been supported by a grant from the Danish Dental Association "Fonden til stCtte for videnskabelige
og praktiske unders~gelser indenfor tandl~egekunsten" and "Dentalaktieselskabet af 1934's
Fond" and the Danish State Research Foundation.
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