andreasen1972 healing of periapical lesion

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, regen-
eration 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 peri-
apical surgery include repair of all perio-
dontal components: cementum, periodontal
ligaments and bone.
Our present histologic knowledge of the
capacity and mode of healing of the perio-
dontium after endodontic surgery is rather
limited and is based on case reports which
deal mainly with unsuccessful cases (Kron-
feld 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 perio-
dontium after endodontic therapy.
MATERIAL AND METHODS
The material consisted of 70 biopsies including
the root apex and surrounding periapical tis-
sues 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 prac-
tice limited to oral surgery.

HISTOLOGIC HEALING AFTER ENDODONTIC SURGERY 149
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 se-
lected 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, includ-
ing 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 for-
malin and later demineralized in formic acid/
sodium citrate. If retrograde amalgam fillings
were present, these were removed after de-
mineralization with a needle or a bur. The
specimens were embedded after double infiltra-
tion in ceIloidin-paraffin. Forty-seven speci-
mens were cut in the mesio-distal direction
along the axis of the tooth, whereas the remain-
ing cases were sectioned in a vestibulo-lingual
direction. Step serial sections were made in 43
cases (Stanley 1957); 27 specimens were sec-
tioned 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 (Andrea-
sen & Rud 1972).
RESULTS
The histological evaluation revealed three
post-operative conditions of the periodontal
ligaments and supporting bone: (1) healing
with re-formation of the periodontal mem-
brane or ankylosis, and no or mild periapica[
inflammation, (2) healing with fibrous tissue
(scar tissue) in communication with or adja-
cent to the periodontal ligament, occasional
ankylosis, and varying grades of inflamma-
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
Type o/ teeth
35-44 45-54 55-89
24 8 5
Maxillary
Type: 1 2 3 4 5 6
Number: 9 31 6 3 7 0
Resection of root and type of root filling
Resection Resection
Retrograde Orthograde
Amalgam Guttapercha
20 37
Mandibular
Type o/ periapical lesion
1 2 3 4 5 6
8 3 3 0 0 0
Apical curettage
Orthograde
Guttapercha
13
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 5 6 7 8 9 10
Number: 3 18 13 11 3 4 7 5 2 0 1
2 acute
11 12 13 14
0 2 0 1

150 ANDREASEN AND RUD
Table 2. Histologic changes found in 70 cases after endodontic surgery
Healing Healing Periapical
with with inflam-
re-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
0 7 4
I 13 15
5 6 4
3 9 0
1 1
Root resorption and
cementum repair Cementum formed without previous resorption 5 8 1.0
Cementum formed after
previous resorption 4 4 9
Resorption arrested 0 15 5
Active resorption 1 8 0
Not evaluable 0 0 1
Ankylosis Present
Not present 2 3 0 8 32 25
Bone marrow Fat marrow
Fat and fibrous marrow
Fibrous marrow
Not evaluable
5 8 1
0 3 0
3 7 9
2 17 15
Epithelial
proliferation Present Not present
0 5 14
i0 30 II
Inflammation No
Mild
Moderate
Severe
2 4 0
8 14 0
0 10 4
0 7 21
tion, and (3) moderate or severe periapical
inflammation without scar tissue.
The 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
Ten teeth were examined histologically in
this group (Table 2). In five cases the re-
sected root surface showed complete repair
with new cementum (Fig. 1). The thickness
of the new cementum was found to decrease
from the lateral to the central parts of the
resected root surface. The new cementum
was most often acellular. In five 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 151
areas. No 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 perio-
dontal 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 re-
generation 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 com-
ponents (Fig. 5). Where scar tissue was
found adjacent to the root surface, cemen-
tum repair was partial in 13 cases and mis-
sing 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 perio-
dontal 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 epi-
thelium was found in the periapical soft tis-
sues or partly covering the root surface. In
one case this epithelial lining was one to
two cell layers thick only, and no inflam-
matory changes were found in the adjacent
connective tissue (Fig. 7). In 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 granula-
tion 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. In 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 ANDREASEN AND RUD
Fig. 1. Healing with re-formation of the periodontal ligament, and a mild periapical inflamma-
tion, A, condition of maxillary second premolar immediately after surgery. B, radiograph at fol-
low-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 perio-
dontal 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 fol-
low-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.