osseous repair of the postextraction alveolus in man

8/9/2019 Osseous Repair of the Postextraction Alveolus in Man

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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 oc-

curring 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 condi-

tions.lO

In a survey of the literature, no reports could be found describing human

histologic materia l 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


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

.Innc. l )ti(i

Patient

Iostoperatil;e days OIL which

oxytctmcycline 1c~1.sgiven

intramuscularly

Postoperative day biopsy

specimen was taken

1 I

(

I) 7,

8 15

1.:

Z 9,

10 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~SCSn 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 from Tissue Hank, UIlited States Naval Medical Sicl~ool,

Fatioual

Naval Metli-

~a1

(knter,

Bethesda, Mrl.


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examined and photographed by fluorescence microscopy. Hontinc hcmatosylin-

and-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 tself 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

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

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 speci-

mcu 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.)


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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

il

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.

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.


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Volume 21

Nurnher 6

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. Mag-

nification, x125.)

IGig. X. A ground undecalcified section, photographed under ultraviolet light, of a pre-

molar alveolus labeled with tetracycline I) and 10 days postoperatively. Fluorescence indica-

tive 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


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Fig. 3

Fig. 9. A ground undecalcified section of a premolar alveolus taken from a 21 day pobr-

operative 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 (71 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 P ig.

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).

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 cspcri-

mental animals also occur in ma.n.

2. If further investigation shows these phenomena to bc demonstrable follow-

ing tooth extraction in all areas of the oral cavity, alteration of some of the

hitherto basic concepts of alveolar how healing may hc indicated.


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~olurnc 21

Nurnher 6

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 in-

volving 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 of

tI~(a Naval RIedic*al Resrxrch Institute, Bethesda, Nd.,

1

P gratefully acknowledged.

REFERENCES

3.

2.

3.

4.

J.

6.

7.

8.

9.

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11.

Boyno, Philip J.: A Study of the Osseous Healing of the Post-Extraction Alveolus Utiliz-

ing Tetracycline Induced Fluorescence, Thesis,

Graduate School, Georgetown University,

1961.

Boync, Philip J., and Kruger, Gustav 0.: Fluorescence Microscopy of Alveolar Bone Re-

pair, 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 Investiga-

tion 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.

osseous repair of the postextraction alveolus in man

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