Section

of the

Federal dental services

Osseousrepair of the postextraction
alveolus in man
Philip

J. Boyne, Captain

(DC) USN

NAVAL

MEDICAL

INSTITUTE,

MEDICAL

CENTER,

RESEARCH
BETHESDA,

NATIOSAL

KAVAL

MD.

ecent fluorescent microscopic studies of postextraction healing in dogs have

indicated the existence of hitherto unreported osseous repair phenomena.-3 In
these observations, marked proliferation
of new bone was noted in marrow
vascular spaces at some distance from the healing sockets, in the bone overlying
the mandibular canal, and in various subperiosteal areas. If these tissue responses
are found to exist in man, revision of current concepts of alveolar bone repair
would appear to be indicated. The purpose of this study was to observe histologically, by means of tetracycline-induced
fluorescence, the osseous repair phenomena associated with healing human postextraction alveoli.
INTRODUCTION

The healing of extraction wounds in experimental animals has been studied

in the past by many investigators.4-s
Weinmann and SicheP offered a detailed description of the histologic stages
of extraction healing as follows: (1) formation of a blood clot filling the socket,,
(2) organization of the blood clot by proliferating
young connective tissue,
(3) gradual replacement of the young connective tissue by coarse fibrillar bone,
followed by (4) reconstruction
of the coarse fibrillar bone and replacement of
immature bone by mature osseous matrix.
ClaflinG observed the following chronologic stages in the histologic processes
of healing of experimental extraction wounds in dogs:
1. On the first day postoperatively
the blood clot had filled the alveolus
and the surface of the clot was covered with a fibrin network.
The opinions and assertions contained herein are the private ones of the author and are
not to be construed aa official or reflecting
the views of the Navy Department
or the naval
service at large.

805

806

Boyne

O.A., ON. & 02.

.June, 1966

2. Three days postoperatively

the epithelium had started to prolifcratc
over the surface of the> clot. Osteoclasts ww present at thcl c&rest of
the bone, and fibroblasts hild started to inr-adc th(l clot from the \valls
of the alveolus.
3. After 5 days the first cvidenec of new bone formation was ohservcd
at the fundus of the socket.
4. At 11 days new bone was evident. along the lateral aspects of +hc
alveolus.
5. At 19 days new bone had reached the crest of the alveolus but the
central portion of the socket had retained the original clot.
6. Twenty-eight
days postoperatively
the alveolus had filled with new
bone.
Although different investigators have observed changes which vary slightly
in time sequence from the preceding description,!, lo this carlv work has been
considered a basic criterion for evalua.tion of extraction wound healing in the
dog.
R,ecently, however, fluorescent microscopic studies of alveolar bone healing
in dogs have indicated the existence of additional histologic phenomena occurring in areas surrounding
the healing socket proper. These phenomena
(termed extra-aZveoZur changes since they occurred outside the alveolus) were
manifested as areas of osseous proliferation
along the lingual aspect of the
edentulous ridge, overlying the mandibular
canal, and in Rdjacent marrow
vascular spaces.
From a chronologic aspect, the observations made in our animal studies did
not support many of the findings previously reported in the lit,crature. For
example, tetracycline labeling indicated that the first bone formed as part of
the healing response to tooth extraction in dogs was not in the socket itself but,
rather, in the described extra-alveolar areas. Later in the healing process, the
first bone seen to form in the socket itself was often found along the lateral
margin of the socket and not in the fundus of the defect.
Considerable difficulty, however, was anticipated in the extrapolation of these
observations to the healing process involved in clinical human postcxtraction
alveoli. The problem of relating the results of animal experimentation
to the
healing of oral surgical defects in ma.n has always been complicated by the
paucity of human histologic material. During the past few years human biops;
material obtained for histologic study has consisted for t,he most part of trephined
or core type specimens which have represented only a portion of the healing
socket area., I1 In those few instances in which specimens have included block
sections of surrounding bone, the tissues have usualIF been obtained at autopsy
and have represented osseous healin g under less than optimal systemic conditions.lO
In a survey of the literature, no reports could be found describing human
histologic material containing the entire healing alveolus and surrounding bone
taken from healthy clinical patients. In order to obtain a better understanding
of the interrelated histologic processes involved in postextraction healing, it was
considered imperative that an attempt be made to evaluate human biopsy

specimens which reflect not only tissue changes in the socket itself Ijut also
tissue response in the surrounding alveolar bow.
METHOD

Twelx clinical patients between the ages of 20 and 45 y2m3, prcscnting

for extraction of all remaining maxillary teeth, were selected for this study in
which the alveolus of the maxillary first premolar was utilized. The tooth was
removed 11sforceps in a simple extraction procedure (Fig. I). An effort. was
made to minim&x all traumatic influences. No mncoperiosteal fiap was raised
and no antibiotics were administered, either systemically or topically, at the
time of the extraction. On tither side of the first, prrmolar, all teeth scheduled
for removal as part of the previously planned full-month cstraction wrc allo~~~l
to remain during the period of observation of hcaling of the premolar alveolus.
Each patient received oxytetracycline intramusrnlarly in two consecutive
daily doses of 4 ing, pm* kilogram of body n-eight, at 5 prcdctcimincd time

Fig. 1. The first premolar in eaxh case was atraumatically removed. So sutures wre
placed: and the alveolus was allowed to heal in a routine manner.
Fig. $. Following a period of postoperative healing, the remaining teeth on either side
uf the first premolar socket were removed. A water-cooled bur (at right) will brt used to
section a bone specimen containing the healed first premolar alveolus.
Fig. 8. Following removal of the biopsy specimen, freeze-dried homogenous bone particlrs
(arrow) rrere implanted into the surgically created defect in order to restore lost contour.
The mucoperiosteal flap will be closed over the graft material.
Fig. 4. Postoperative healing was uneventful in all cases. This is a view of the graftctl
surgical site shown in Fig. 3, taken 3 weeks postoperntircly. Normal contour has been rcstorwl
to the edentulous alrcolar ridge.

808

Rope

0,s.. O.JI.&k 0.1.

.Innc. l!)ti(i

Iostoperatil;e
oxytctmcycline

Patient

days OIL which

1c~1.sgiven

intramuscularly

Postoperative

day

biopsy

specimen was taken

1 :I

(
I)

7,

1.:
!Z

9, 10

15

1;

postoperatively
(Table I). One week following administration
of the antibiotic,
the remaining teeth in the involved quadrant were removed (Fig. 3). Following
the elevation of an cstcnsive mucoperiosteal flap, a block section of alveolar boric
was removed with a water-cooled bur (Fig. 2). Both cortices were removed wit,h
the spccimcn containing the entire socket of the first premolar. The superior cut
separating the specimen from the remaining maxillary
bone was made at a
distance of approximately
3 mm. above the apex of the socket in order to include>
:I portion of the pcriapical bone in this region (Fig. 3).
The bony defect remaining after biopsy was implanted with freeze-dried
homogenous cancellous bone particles
and the mucoperiosteum was closed
(Fig. 3). The postoperative course was uneventful
in all cases. The alvcolel
ridges healed with excellent contour and width following excision of the biops>
specimens (Fig. 4). Dentures were inserted during the forth postoperative week.
(Biopsy specimens were obtained with the assistance of Dr. Jaime Yrastorza of
\\rheatridge Colorado, formerly of the Veterans Administration
and (:corgetown
lhiversity.)
The patients were divided into six groups, so that two specimens
were obtained for each increment of post,operativc labeling according to Table 1.
The maxillary first premolar site was selected for this study because of the
relative ease with which surrounding
osseous tissues could br excised without,
endangering the integrity of important. adjacent anatomic structures. An effort
was made to avoid the maxillary antrum by selecting only those C~SCSin which
t,here was a high antral floor.
In two instances, however, in spite of these precautions, the maxillary sinus
was entered inadvertently
during removal of the biopsy spccimcns; healing was
~~ncventful in both cases. Ground undecalcified sections were prepared from the
specimens according to :I previously described method,l- and thp slides wcrc~
Obtained

~a1

from

Tissue Hank, UIlited

(knter, Bethesda, Mrl.

States Naval

Medical

Sicl~ool, Fatioual

Naval

Metli-

examined and photographed by fluorescence microscopy. Hontinc hcmatosylinand-eosin-stained dccalcifird sections were also prepared and corrrlatcd with
ground spccimcns.
RESULTS

Specimens taken from patients who had been given oxytetracyclinr on the
fifth and sixth postextraction days exhibited very minimal fluorescent labeling
of new bone in the surrounding marrow vascular spaces.There was a complctc~
absenceof fluorescent new bone matrix in the socket itself and along suhpwiostcal
areas of the alveolar ridge (Fig. 5).
Specimens tagged at 7 and 8 days demonst,ratcd fluorescent new hone in thca
marrow wscular spaces adjacent to and along the entire length of the lamina
dura.. IIowercr, there was no labeled bone formation in the socket itself (Fig. 671.
The first c\-idcncc of calrified osseousmatrix seen in the healing of the human
cxtrsction sock&, therefore, was located outside the alveolus and could be termed
a part of the extra-alveolar response to the surgical procednrc. This osscons
rrpair, which had hcgun on the scrcnth and eighth postopcratirc day. ws still

Fig. 5

Fig. 6

Ag. 5. il ground undecaleified specimen taken 13 days after extraction of the premolar.
The patient received tetracycline on the fifth and sixth post,extraction days. Under ultraviolet
illumination, there is minimal fluorescence, indicating ne~ hone growth in the surrounding
marrow vascular spaces (arrow)
but no new bone in the socket itself (81. (Magnification,
X10.)
Fig. 6. A ground undecalcified section of a specimen taken 15 days postoperatively ant1
labeled by tetracycline on the seventh and eighth postoperative days. The view of the specimcu photographed under ultraviolet light on Panatomic X film illustrates the palatal wall
of the alveolus. Fluorescing new bone is seen on the marrow vascular side of the lamina dura
along the entire extent of the palatal wall of the socket (arrow). Osseous repair also involves
the crestal area (C). This osseous response occurred prior to formation of honr in the socket
(8) itself. (Magnification, x10.)

in progress on the fifteenth day, as indicated by the presence of acti\c

osteohlasts lining the trahrculae of t,hr marrow vascular spaces adjacent to the
Iamina dura (Fig. 7).
Specimens labeled on the ninth and tenth days dernonstrat,ed flnorescent new
bonr, not only in the marrow vascular spaces but also in the socket proper along
the lat,eral aspect of the alveolus. Thus, the first cxidencc of new bone formation
in the socket itself was seen IO days postoperatively
(Fig. 8).
Specimens lab&d
on t,hv twelfth postextraction
day also indicated thc&
prescnccl of new boric alon, 0 tllc lateral wall of the socket, and in adjacent~ I)OI~P
IliIS.
Subsequent new bone repair hat1 continued until the nineteenth postoperative
day,
when the biopsy specimens were taken. This latter increment of bone
I\l;ltris had filled a large port,ion of the socket.
Specimens labeled on the thirtrcnth
and fourteenth days after clstraction
~~cvealcd a deposition of boric along the lateral wall and t,hc fnndus of the
socket, (Fig. 9). The tagged bone occupied approximately
one-third of the cntirc
bony al~colus. Thus, it would appear that vhile the first bone Formed in the
sock& lnily not necessarily be located in the fundus of the defect-and,
indcccl,
is more often to be found along the lateral wall-the
propensity for bone repail
in the fundus is manifested in later healing stages. Bone formation in endostcal
spaces was also marked in specimens labeled 2 weeks postoperatively
(Fig. 10).
Specimens labeled on the fifteenth and sixteenth days closely resembled those
taggca 2 weeks postoperatirely.
il

DISCUSSION

The results of this study of biopsy ma,terial taken from healing human
maxillary
premolar postcxtraction
al\-coli have led to several observations
which arc in conflict with widely held concepts of extraction healing.
The first bone formed as part of the repair response was not in the socket
itself but, rather, in the surrounding
marrow vascular spaces. This was
particularly
midcnt, along the marrow \-ascnlnr sitlc of the lnmina dura (Figs.
C,and 7).
Boric formation in the socket was first observed in spccimcns labeled 9 ancl 10
days postoperatively.
This first apposition of new bone was seen along thv
lateral wall of the socket and not in the fundus (Fig. 8), as has been frcquentl!
reportcd.~ I Specimens tagged 2 weeks after extraction demonstrated a conelikc
area of bone formation cstcndin g along the lateral walls of the alveolus to
include the fundus of the socket (Fig. 9). Some illustrations
of socket healing
in reports contained in the literature would appear to represent this approximate
stngc in the healing process. The particular configuration of the osseous repair
at, this stage can easily lead to the impression that the bono proliferation
began at
the a.pes of the socket when, in rcalit.v, it may well have started along t,hr
lateral alvco1a.r walls. The valur of the application
of investigative
surgical
techniques inl-olving intrayital
stainin, u is thus apparent. By chronologically
orienting the osseous repair patterns, it has been possible to record t,hcse tissue
rwponscs

nccuratcly

ilS

to position

and

time.

Volume

21

Nurnher

Osseous repair

of postextraction

al~*edus

81 1

F%y. 7. A decalcified section taken from the specimen shown in Fig. 6. The palatal lamina
dura extends diagonally
across the s&ion.
On the right, trabeculae
(arrow)
can be seen
extending into adjacent marrow vascular spaces (UV),
NW bone in this area was shown by
tetracycline
labeling to have begun 7 and 8 days postoperatively.
Minimal
osseous formation
is seen on the sock& side of the lamina dura (A). This portion of thcl palatal ~a11 of the
socket was taken from the crrstal third of the alveolus. (IIematoxyliu
and rosin stain. Magnification,
x125.)

IGig. X. A ground undecalcified

section, photographed
under ultraviolet
light, of a premolar alveolus labeled with tetracycline
I) and 10 days postoperatively.
Fluorescence indicative of new bone formation
is demonstrable
on the soekct side (S) of thca lamina dura along
the entire extent of both buccnl and palatal walls of the alveolus. Such labeling at 9 and 10
days demonstrated the first evidence of osseous repair in the socket itscalf. (Magnification,
x10.1

Fig. 3

Fig. 9. A ground undecalcified section of a premolar alveolus taken from a 21 day pobroperative biopsy specimen demonstrates the effect of tetracycline labeling on this tlurtecnth
and fourteenth postextraction days. Two of the first premolars cxtraeted in this srriw pw
sented bifurcated roots. Tn this spwimen, both the alveolus of the buccal root (71I and thr
alveolus of the longer palatal root (7) demonstrate fluorwing
nmv bone formation in thtx
fundi and along the lat,eral socket walls. Thrrc is alsn evidence of osseous proliferation along
the interradicular septum. A large void in the bone (E / dlich rcwmblcd the maxillary antral
floor proved to be an endoatcal space. The margins of this space clxhibited a mnrkc~tl prolifcrn
Con of new bone as part, of tlir hraling rrsponw. (Magnification, x10.)
Pig. IO. A section taken from the specimen shon-n in Pig. 9. The large void which oval;
located above the premolar socket and which rcsomblell the maxillary antrum is seen in this
section to be in reali@ a large endostoal space. Row of ostcohlasts (arrow) are present along
the margins of the space. New bone matrix formation in this arca was shown by tctracyeliuc
labeling to have been active 13 and 14 days after tooth c~xtraction. The persistent osteoblsatic
activity at the time of biopsy, 21 days postoperatirrly,
~vouhl suggest a strong sustained
tendency toward endosteal bone formation throughout this part of thr process of osswus 11~1
ing. (Hematoxylin and eosin stain. Magnification, x201).i

The dynamic nature of bone formation in the marrow vascular spaces (Figs.
7 and 10) suggests a strong t,cndency toward sustained apposition of bone in
these areas as an apparently compensatory mechanism of repair.
Subperiosteal apposition of hone along the lingual cortcs, although not as
marked as in some laboratory animals, was nercrtheless present,. This area of
bone repair may also reprrsent a.compensatoy healing response.
CONCLUSIONS
1. The results of this study tend to indicate that certain extra-alveolar and
intra-alveolar repair phenomena observed in postextraction healing of cspcrimental animals also occur in ma.n.
2. If further investigation shows these phenomena to bc demonstrable following tooth extraction in all areas of the oral cavity, alteration of some of the
hitherto basic concepts of alveolar how healing may hc indicated.

~olurnc

21

Nurnher

Osseozhs repair

of postextraction

alveolus

813

3. This work serves to emphasize the exceedingly complex mechanisms

involved in extraction-socket
healing. The bony alveolus produced by tooth
removal does not heal by a simple process of omeous proliferation
from the
fundns to the crest of the defect. In reality, the surgical procedure has produced
a compound wound which heals by a series of complex osseous phenomena involving not only t,he socket itself but other important anatomic areas as well.
4. It is belieTed that the development of esodont,ia techniques of the future
should be predicated on a concise understanding of the histologic healing process
that follows this most, common of oral surgical procedures.
The teclmical assistanec provided I)y J. Smith, DT-?, USh, and Mr. Clarence W. Miller
acknowledged.
tI~(a Naval RIedic*al Resrxrch Institute,
Bethesda, Nd., 1P gratefully

of

REFERENCES
3. Boyno,

2.
3.
4.
J.

6.
7.
8.
9.
10.
11.

Philip J.: A Study of the Osseous Healing of the Post-Extraction

Alveolus Utilizing Tetracycline
Induced Fluorescence,
Thesis, Graduate School, Georgetown University,
1961.
Boync, Philip J., and Kruger, Gustav 0.: Fluorescence Microscopy
of Alveolar Bone Repair, ORAL SURG., ORAL MEU. & ORAJ, PATH. 15: 265-281, 1962.
Boyne, Philip J.: Fluorescence Microscopy
of Bone Healing Following
Mandibular
Ridge
Resection, ORAL SURG., ORAL MEI). 6c ORAL PATH. 16: 749-756, 1963.
Alling, C. C.! and Kerr, D. A.: Trauma as a Factor Causing Delayed Repair of Dental
Extraction
Sites, J. Oral Surg. 15: 3-11, 1957.
Amler, M. H., Johnson, P. L., and Salman, I.: Histological
and Histochemical
Investigation of Human Alveolar Socket Healing in Undisturbed
Extraction
Wounds, J. Am. Dent.
A. 61: 32-44, 1960.
Claflin, I&. S.: Healing of Disturbed and Undisturbed
Extraction
\Vounds, J. Am. Dent. A.
23: 945-959. 1936.
Schramm, I+. R.: A Histologic
Study of Repair in the Maxillary
Bones Following
Surgery,
J. Am. Dent. A. 16: 1987-1997, 1929
Simpson, H. E.: Experimental
Investigation
Into the Healing of Extraction
Wounds in
Macaeus Rhesus Monkeys, .T. Oral Surg., Anesth. & Hosp. D. Serv. 18: 391.399, 1960.
Weinmann, J. P., and Sic&r,
H.: Bone and Bones, St. T,ouis,, 1955, The C. V. Mosbv
Company.
Mangos, .T. F.: Thr Healing of Extra&ion
Wounds, Sew Zealand D. J. 37: 4-22, 1941.
Bell, William
H. : Histologic
Study of Heterogenous
Bone Implants
in Human Beings:
Preliminary
Report, J. Oral Surg., Ancsth. $ Hosp. D. Serv. 17: 3-13, 1959.