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Contribution of autogenous condylar grafts to mandibular growth
Research Contribution of autogenous condylar grafts to mandibular growth Sidney Peskin, Chiccl.go, Ill. DEPARTMENT
D.D.S.,
OF ORAL
DENTISTRY,
AND
UNIVERSITY
OF
and Daniel
M.S.,”
AND
DEPARTMENT
11. La&in,
MAXILLOFACIAL
SURGERY,
OF
COLLEGE
SURGERY,
D.D.S.,
COLLEGE OF
ill.S.,‘*
OF
MEDICINE,
ILLINOIS
T
he mandibular condyle is the most important growth center of the mandible.6p 221-25Through interstitial and appositional growth of cartilage in this area, both the height of the ramus and the over-all length of the jaw are increased. Injury to the condylar growth center, whether congenital, traumatic, or inflammatory, can thus produce marked mandibular deformity. This is USUally characterized by the development of antegonial notching, a short and wide ramus, and a shifting of the mandible to the affected side.F3 ** Although experiments on the restoration of lost mandibular growth have been limited,s, 27 a considerable number of studies have been done on the problem of growth arrest in the long bones. These have included investigations on both animals and human beings. The results of Helferich,l* Rehn and Wakaof bayashi,*O Straub, 26 Herndon and Chase,13 and Fohls indicate the feasibility such surgical procedures as epiphyseal transplantation to restore longitudinal growth. The purpose of this investigation was twofold: (1) to evaluate the amount of growth potential which remains after partial removal of the condyle and (2) to determine whether autogenously transplanted condylar growth centers can restore the growth of the mandible after condyloidectomy. The results, based on gross observations and histologic examination, show that the dog condyle retains a major portion of its growth potential, even after partial resection, and that autogenous condylar grafts can be used to restore mandibular growth. This investigation w&5 supported Health, United States Public Health *Instructor in Oral Surgery. **Professor and Associate Head,
by Research Service. Department
Grant
of Oral
DE-01849,
and
National
Maxillofacial
Institutes
of
Surgery.
517
518 REVIEW
l'cskitr
tr~id l,fldi~~
0,s.. O.Jl. & 0.1'. 0~~101 wr,
1!Mz
OF THE LITERATURE
Allh0llgh tll~ tfl’c~c*ts01’mantlih~llat~ Il(~llii~orti~~IectoH1~. II;LVC:1101IKY~IIst uclicd, thta roslllts ot’ ct~I~tlylect.tmky hrvr bcrn cd~m3iwly invcstigatd in both animals ELIlclIklall. Nngcl and Krotlic” noted that in human subjects loss of the condylar groWtl1 Celltrr rcsult,ed in ~IltPg()rli;ll not~hirlg, shiftin, w of the nrandiltle to the affected side, fullness of the face, a,nd development of a short and wide ramux. In animal expcrirnents, Sarnat and ISr~gel~~evaluated tht: results of condylectomy in monkeys. Their findings were comparable to those seen in human bcings. Jarabak15 observed grossly that various amounts of regeneration occurred after condylectomy in young rats, with little or no deformity. Kcndrick, Carncron, and Matthews” removed small sections of the postcrosnpcrior ramal surface, including part of the condyle, in monkeys, Sinccl this procedure included only a vcrp small part of tht : growth center, no effect on growth was noted. In experiments in which the condyles were fractured and dislocated, thus eliminating their contribution to growth. Walker,‘!’ using young monkeys, found regeneration of t,he cond.vlc with only slight growth disturbance. His obsrrvat,ions were based on gross and histologic examination. Jarabak and Stuteville,‘” using a young monkey, obscrvc>dan antcriorlp opened bite and antegonial not.ching, but they also found no appreciable changes in facial growth. Heurlin, Gans, and Stutevillc’” found that, mhcn this same procedure was performed on older monkeys, marked deformities were produced. Thcsc included a decrease in total facial height and a shifting of the mandible to the affected side. The first cxpcrimental attempt, at determining the possibility ot transplanting growth cartilage was made by Helferich,‘2 who cstiscd and reimplanted the lower cpiphysis of the ulna in rabbits. His results showed retention of the property for producing longitudinal growth. .Endcrlcn” made microsco’pic sections of Hclferich’s preparat,ions and found that, the epiphyseal region retained its vit,alitp to a large cxtcnt. In 1912, aftcxr Axhausenl showed that epiphyseal cartilage with its pcrichondrium could survive transplantation, R,ehn and Wakabayashi’” transplanted the head of the radius in rabbits and showed that, it maintained its histologic structure and it,s capacity for longitudinal growth. Fohl” likewise transplanted epiphyseal cartilage in rabbits with excellent rcsult,s. More recently, Herndon and Chase,‘” after a series of homogenous and autogenous joint transplants in dogs, concluded that nutogcnous grafts of epiphyseal cartilage survive while l~omogcnousgrafts are completely resorbed. Contrary to t,he preceding reports, Haas’O reported in 1915 that transplantrd epiphysrs did not contribute to longitudinal growth o-f bones. He repeated his work in 1931’l and confirmed his previous results. Kisgard2 removed sections of the tibia in goat,s and autogcnously transplanted epiphyses to the area. Since no new growth occurred, hc was also opposed to the procedure of’ c$physeal transplantation. Woodruff,“’ after HII extensive review of the subject, concluded that re-establishment of growth in a bone by autotransplantation of a growth center has met with varying results but that, since some successful caseshave been reported, this should stimulate further investigation into the subject. After Fohl” encouraged the transplantation of epiphyseal cartilage in man on the basis of his and other animal expcrimcnts, some clinical cases began to
bc reported. In 1912 StrautP grafted an epiphysis and diaphysis to compcnsatc for loss of the tibia1 cpiphysis from osteomyelitis. The patient was 61/z years old at the time of the surgical procedure. On the basis of gross and radiographic examination made 17 years later, the graft appeared to have survived and growth had proceeded in a normal manner. JVengcr,“” in 1945, reported a case in which he transplanted the cpiphysis and part of the diaphysis of the fibula to the first metatarsal in a 7-year-old patient. The deformity was torrectcd, and the transplant functioned physiologically. Bttempts at correction of the disfiguration caused by loss of the growth center in the mandibular condyle have been mainly in the realm of esthetic reconstruction rather than restoration of growth. Kazanjianl’ used a tibia1 bone graft and advised this method for older patients in whom no growth could be expected. Roy and SarnaP suggested the use of costochondral junction grafts in young patients, with the idea of growth occurring from the graft. No clinical cases in which this method has been used have been reported. Stutevillc and Lanfranchi*’ used the proximal third of the metatarsal in a young girl to replace a hppertrophied condyle. The function of the jaw improved immediately, but the growth aspect of the treatment was not evaluated. Entin* used the metatarsal-pha.langeal joint attached to the mastoid process and the mandible in a case of aplasia of the condyle and ramus. Esthetics were improved but no growth occurred. Up to the present time, there have been no reports of either clinical or experimental studies in which autogenous mandibular condyle grafts were used to restore growth of the mandible. MATERlAL
AND METHODS
Thirty-one dolichocephalic puppies, weighing between 4 and 13 pounds each, were used in this study. Their ages, as determined from the dentition, ranged from 6 to 12 weeks. Each dog was given an intramuscular injection of 300,000 units of benzathine penicillin 2 days preoperatively. At the time of the surgical procedures, the animals were anesthetized with intravenous pentobarbitd sodium. Both sides of the face were shaved, washed with hexachlorophene soap and sterile water, and rinsed with 1:750 benzalkonium chloride. The surgical approach to the temporomandibular joint was the same in each dog. A vertical skin incision was made over the mandibular ramus, extending from just above the zygomatic arch to the inferior border of the mandible. The underlying masseter muscle was separated, exposing the joint capsule. This was incised vertically and the margins were retracted, revealing the articular disc. The attachment, of the disc to the outer aspect of the condyle was then cut to allow lateral dislocation of the mandible. Three types of operation were performed. In Group I (thirteen animals) the lateral half of the condyloid process was removed unilaterally (hemicondyloidectomy) (Fig. 1) _ A No. 700 bur in a dental handpiece was used for this procedure. On the opposite side, a sham operation was performed; a similar approach was made to the temporomandibular joint, but no resection was done. The resected portion of the condyloid process was implanted in a subcutaneous pocket prepared in the anterior abdominal wall.
Group I:
Group II:
Fig. 1. The surgica1 procedures performed on animals in Groups I and II. the color of the graft indicates its original source. Note that the transplantation requires that the grafted portion of the condyle be rotated 180 degrees.
In
Group II procedure
In Group II (twelve animals) the lateral half of the condyloid process was removed bilaterally (Fig. 1). In addition, on one side the medial portion of the condyle was also excised. The resected lateral halves of the condyloid processes were then transplanted to the contralateral sides. They were fixed in position with a transosseous stainless steel wire (0.012 inch in diameber) placed through small bur holes made in the mandibular neck and the transplant (Fig. 1). In Group III (six animals) unilateral condyloidectomy was performed. This served as a control experiment to verify that surgical interference with the condylar growth center of the dog would result in mandibular deformity. Metallic implants were inserted bilaterally into the mandibles of animals in all three groups to provide stable landmarks for direct craniometry. Prior t.o completion of the temporomandibular joint surgery, two small bur holes, one above the other, were made in the bone just inferior to the stump of the condyloid process with a No. 1, round dental bur. A third hole was placed in the body of the mandible near the mental foramina (Fig. 2, A). This was aecomplished through a small incision in the skin and periosteum. After the holes were filled with dental amalgam, the distances between them were measured with a Boley gauge. These measurements were accurate to within 0.1 millimeter. Upon completion of the entire operation, the periosteum and subcutaneous tissues were approximated with 4-O chromic catgut sutures and the skin was
Volume Number
Fig. measured. sured.
dutogenous
20 4
1. A, The positions B, The landmarks
of the metallic used for the
implants mandibular
conclyla~ grafts
placed in the mandible measurements and
521
and the distances the distances mea-
closed with 3-O silk sutures. All incisions were sprayed with a plastic agent (Rezifilm) . Procaine penicillin G, 300,000 units, was administered intramuscularly immediately after the surgical procedure and for 2 days postoperatively. In addition to their normal diet of 50 per cent Purina Dog Chow, 25 per cent Miller’s Puppy Meal, 25 per cent cooked canned horsemeat, and sufficient water to hold the ingredients together, the animals were provided with whole milk for one week postoperatively. Additional drinking water was also provided ad libitum. Two dogs from Groups I and II were killed at intervals of 4, 8, 12, 16, 20, and 24 weeks.* All the animals in Group III were killed after 6 months. After each animal was killed with a lethal dose of pentobarbital sodium, injected intracardially, the head was removed, skinned, and placed in 30 per cent formalin. *A single dog in Group craniometric analysis.
I was also
killed
at 2 weeks.
This
animal
was not
included
in the
Following fixation, the amalgam nii~ik~rs wcr~~ esposc~l illltl cliroc4 tll(~iisI11’+ ments were made bttwcon t hc markers. An addit ional group of int’ils1ir(meiits were also made on each msndible bilaterally (Fig. 2, 11) These inc~ludcd the over-all length oi’ the mandibltt as m(2~suretl fi*orn tlio lllost superior point 011 the alveolar prorcss at the symphysis to the most postcbrior point on the: c~ondyl(~ (A) and from this same s,vmph~-s(lalarea to the most posterior l)oint on thl\ angular process (B) ; the height of the bod,v of the mandible as ~~~cw~wt~d from the inferior border to the alveolar margin in the region of the major mental ~OIXITICII (C) ; the height of the ramus as measured from the tip of the coronoid process on a line perpendicular to the inferior border (I)) ; thcl most postcrioia point on the condylc to the posterior margin of the major mental fo~arno~~ (14:) ; the most posterior point on the condylc to the most postrrior point 011the angular process (F) ; the tip of the coronoid process to the most posterior point on the condylc (G) ; the anterior border of the ramus to the posterior border of the ramus at the level of the most posterior point on the c~~nd~la (II) ; the posterior border of the ramus to the most posterior point on the cond,vlc (I) ; and the posterior margin of the major mental foramcn to the most superiol point on the alveolar process at the symphgsis (J). For the histologic aspect, of t,he stud,v, the condyloid process and the SUP rounding tissues were excisrd from the skull en bloc by means of a. coping saw, mallet, and chisel. The specimens were decalcified in a solution containing equal parts of 50 per cent formic acid and 20 per cent sodium citrate. When radiographs showed that the bone was decalcified, the specimens wcrc washed, tlchydrated, and infiltra.ted with crlloidin. Serial sections wcrc stained with llenliltoxylin and eosin and mounted on slides with synthetic mountinK rcGn ant1 XJkllP.
RESULTS Gross
observations
All of the animals were examined 4 days postoperatively, and it, was found that two dogs in Group I had some purulent drainage from the preauricular incisions. One week postoperatively, however, when the skin sutures were rcmoved, none of the animals showed any evidence of infection and all incisions were clinically healed. The dogs generally exhibited moderate edema and limitation of mandibular function for the first 2 weeks. In the animals killed between 2 and 4 weeks, this limitation was evidenced by the presence of gross calcareous deposits on the teeth. In the animals subsequently killed, only slight amounts of calculus were found. After the second week food consumption began to increase and mandibular function improved. By the third to the fourth week, the animals again began to gain weight. Mandibular function appeared normal at that t,ime. On exploration of t,he abdominal area at the time of death of the CY’OLI~ I dogs, none of the tr.a,nsplantetl portions of the condgle were found, although healing of the incisions appeared normal. It was thought that, the transplants had been resorbed since only a fibrous mass remained. No grossly visible changes in the shape of the mandible were noted at any
Autogenous
co~~dylnr
grafts
523
time in dogs of either Group I or II. ROWC~C~,some minor oeclusal irrcgularities were observed. In the 4-, 8-, and 12-week specimens of Group I, the mandible had shifted somewhat to the side of the hemicondyloidectomy. The mandibular teeth on the unoperated side were slightly lingual t,o their normal position in relation to the maxillary teeth. This deformity was not present in the 16-, 20-, and 24-week specimens. The 4-, 8-, and E-week specimens in Group II displayed the same deformity as seen in Group I, with a shift of the mandible to the side of the condyloideetomy and contralateral graft. This was not observed in the older animals. In Group III all of the animals showed a marked shift of the mandible to the side of the condylectomy. The posterior teeth remained in occlusion, but in the incisor region the midline of the mandible was skewed to the operated side (Fig. 3). Some gross changes in the shape of the mandible were noted in this group. The depth of the notch anterior to the angular process was increased on the operated side. Likewise, the height and thickness of the body of the mandible were increased. Craniometry
Most of the metallic implants in the animals killed between 4 and 12 weeks remained in the bone and maintained the samepositions as at the time of surgical intervention. In the animals killed between 16 and 24 weeks, however, the posterior markers were frequently found in the masseter muscle. This was a result of growth and remodeling of the ramus. In these instances measurements could not be made. In Group I the 4-, 8-, and 12-week specimens showed a slight underdevelopment of the mandible on the side of the hemicondyloidectomy. The over-all length as measured from the condyle to the symphysis was always less than on the control side (Table I). The distance from the angular process to the symphysis was also less, as was the measurement from the condyle to the angular process. The height of the coronoid process and the width of the ramus, how-
Note
Fig. 3. The relationship of t,he anterior teeth the shift of the mandible to the operated
at the time side.
of death
in a Group
111
animal.
-______
._ l’ime
Dog
after surgery (weeks)
._..
~._
___~_._
l)ifl’wenr:cs
.--.--
-.----.-.---~-----
.._...
-~ -.
bc1wrc
-~---~
.~
71 ,nc~nsu,~~?n~llts”
--~-~
!
~.--T-
A
B
CID
E/
lFIG!
laj
I
- ----~~-~-
1
T/J
:
: 3
4 i
2.7 2.9 2.1
2.2 2.4 1.2
-0.1 0.1 -0.1
-1.3 0.9 0.7
2.1 2.5 1.8
1.6 1.8 1.2
-0.2 0.1 -0.1
0.3 0.2 -0.2
0.20 -0.1
0.2 0.1 -0.1
: 6 ;
1% 12 16
2.2 0.7 0.6 -0.2 0.7
2.0 0.4 0.5 -0.1 -0.4
if -0:s -0.1 0.1
-0.2 0.2 -0.4 -0.6 0.2
2.2 0.9 0.4 0.6 0.3
1.1 0.7 0.9 -0.5 -0.4
-0.1 0.1 -0.3 -0.1 0.3
-0.4 0.: -0.1 0.3
-;+ -0:” 0.3 0.2
-0.2 0.1 0.2 -0.2 0.1
9 10
20 20
0.3 -1.1
-0.4 0.6
0.1 0.1
0 0.7
-1.0 0.8
0.4 -0.4
-:*y
0.2 -0.3
--0.9 0“
0 n
11 12 -0.2 0.3 -0.3 0.2 -0.4 0.3 -0.40 0:2 -0.2 -0.6 -0:; 24 0.7 -0.5 0.1 -0.1 0.3 0. 1. -0.:’ *All numbers are expressed in millimeters and are accurate to 1 0.1. A negative value indicates that the distance on the control side was less than that on the side of the hemicondyloidectomy. The letters correspond with those shown in Fig. 2, R and indicate the f ollorving measurements : F = Condyle to angular process. A = Condyle to symphysis. 13 = Angular process to symphysis. G z Condyle to coronoid process. C = Height of body of mandible. H z Width of ramus. D = Height of ramus. I z Condyle to anterior ramus. E = Condyle to mental foramen. J = Mental foramen to symphysis.
ever, were not affected by the hemicondyloidectomy. Likewise, as indicated by the random distribution of the differences, the height of the body of the mandible was not changed by this procedure. These changes were not observed in the 16-, 20-, and 24-week specimens. In the Group II animals killed between 4 and 12 weeks, the changes in size noted when side A (condyloidectomy and contralateral graft) was compared with side B (hemicondyloidectomy and contralateral graft) were relatively similar to those seen when the operated and control sides were compared in the young Group I animals (Table II). No significant differences between sides A and B were observed in the 16-, 20-, and 24-week specimens. The Group III animals showed a marked retardation of growth on the side of the condylectomy. The over-all length of the jaw was markedly reduced. On the other hand, the height of the body of the mandible was greater on the operated side when compared to the control. The only measurements that wcrc not affected were those on the coronoid process (Table III). Histologic
observations
Group I. The a-week specimen showed the site of the hemicondyloidectomy to be healing normally. Young fibrous connective tissue was beginning to proliferate over the cut surface of the condyle (Fig. 4). By the end of 4 weeks, this area was completely covered with a layer of fibrous connective tissue. Some membranous bone formation was occurring in the deepest part of this layer. Active differentiation of cartilage cells and endochondral bone growth were continuing in the unoperated portion of the condyle (Fig. 5, A).
Volume Number
20 4
flut0,genou.s
condylar
525
grafts
Table II. Comparison of measurements on the side of hemicondyloidectomy graft with those on the side of condyloidectomy and graft (Group II)
nnO
!Eme after surgery , (weeks)
Differences 2.1
1.5
2.9
3.1 1.1
2.0 1.8
1.1 1.4 0.6 -0.4 0.8
16 76
io
20 24 24
12
measwements*
A\BJCIDJEjFlGIHl
4 4 8 8
7 8 9 10 11
between
2.6 1.2 1.7 -0.6 -0.2
-0.1
-1.0 4.2
0.7 -0.9
0.3 0.9
and
I\J -0.1 0 0.8 0.1 -0.1
1.0
-0.9 0.2
1.7 2.2 1.8
1.0 1.8 1.1
--0.1 0.7 --0.3
0.3
2.1
1.1
0.4
0.3
0.9
0.4
0
-0.1
-0.2 -0.2 0.2
-0.3 0.7 0.9
o".: -0:4
--0.1 --0.1
0 -0.2
-0.4
0.1
-0.1 0 -0.1
-0.6 0 0.2
f$ -0:2 0.4
0
0.3
-0.9
0 0.6 -0.2 0.2 0.2
0.4 0.2 0.2 -0.7 0.2
0.8 -0.4
-0.8
1.0 -2.1 0.1 0.2 0.2
0.7
-0.1 0
1.0
1.8
0.5 -0.2
-0.1
;.,”
-0.3 0.2
0.1 0.8
-0:3
-0.2
0
0 0.3
-0.2 -0.4
0.1 0
0.1
*All numbers are expressed in millimeters and are accurate to 20.1. A negative value indicates that the distance on the side of the hemicondyloidectomy and graft was less than that on the side of the condyloidectomy and graft. The letters correspond with those shown in Fig. 2, B and indicate the following measurements: F = Condyle to angular process. A = Condyle to symphysis. B = Angu!ar process to symphysis. G = Condyle to coronoid process. C = Height of body of mandible. H = Width of ramus. I = Condyle to anterior ramus. D = Height of ramus. E = Condyle to mental foramen. J = Mental foramen to symphysis.
Table Ill. Comparison of measurements on the control side with those on the side of the condyloidectomy (Group III) I Dog 1
I
A
1
B
)
C
Diferences 1 D
j
between, E 1
meaSUTementS*
F
I
G
1
H
I
1
1
J
32
7.2 4.2 7.9
8.1 6.7 3.8
3.9 2.7 4.3
0.1 -0.1 0.7
4.2 4.3 3.4
2.5 4.7
-0.3 0 3 0.5
0.3 -0.90.2
7.9 w3
0.2 0.3
z 6
7.5 ifi::
67 7.2 7:3
4.8 5.1 4.6
-0.30.7 -0.3
$4 3:8
4';i 7 3:4
0'34 1:2
-0.40.7 -0.4
4'2 5:l 8.2
0:s o".i 0.4
*All numbers are expressed in millimeters and are accurate indicates that the distance on the control side was less than dyloidectomy. The letters correspond with those shown in Fig. ing measurements : A = Condyle to symphysis. F = Condyle B = Angu’ar process to symphysis. G = Condyle C = Height of body of mandible. H = Width D = Height, of ramus. I = Condyle E = Condyle to mental foramen. J = Mental
to kO.1. A negative value that on the side of the con2, B and indicate the followto angular process. to eoronoid process. of ramus. to anterior ramus. foramen to symphysis.
The a-week specimens were very similar to those from the d-week group. However, between 8 and 12 weeks there was a great increase in membranous bone formation in the resected area. This new bone formation had resulted in the condylc attaining a. relatively normal outline. The entire articulat,ing surface was covcrcd with mature fibrous conne&ive tissue. However, hyaline rartilagc st,iIl had not re-formed in the deepest layer of the operated side (Fig. 5, B) . In the 16- and 20-week specimens the rescctcd portion of the condyle had
0.5.. 0.11.
1'Hi.i
undergone almost complete regeneration. The lateral port.ion now contained some cartilage cells in the deep layer (Fig. 6, A and B). Fndochondral boric growth was actively occurring. The 24week specimens showed well-formed condyles of the adult type. The surface was covered with a thin fibrous connectivc tissue lqvcr, hencath which was a narrow cartilage laycxr of uniform thickness. There was no longer any significa.nt dcgrec of cndochondral boric formation in thcsc spccimc~ns. CONDYLOIDECTOillY
WITH
CONTR,ZLATERAL
mens bony union had occurred
between
GRAFT
the graft
I). In the I-week speciand the mandibular n~k. The (FIG.
Volurrlr~ Number
20 a
ilutogenous
co,~dylar
grafts
527
Fig. 6. A, Photomicrograph of a 16-~~-eek specimen showing complete regeneration of the structure. (Hematoxylin and eosin stain. Magnification, x6; reclucecl 3h.) B, High-power photomicrograph of the outlined area in A showing cartilage cells in the deep layer of the fibrous connective tissue. (Hematoxylin and eosin stain. Magnification, x350; reduced T/i.)
graft was properly oriented and showed evidence of partieipat.ion in endochondral bone growth. A thin fibrous connective tissue layer covered the area where the medial aspect of the condyle had been excised (Fig. 7, A). This specimen closely resembled the 4-week specimen of Group I. In the EL and 12-week specimens the condyle had a nearly normal outline. This was due to membranous bone formation which had occurred within the fibrous connective tissue in the resected a.rea. There were now some cartilage cells in this layer (Fig. 8, A and 13). The 16- and 20-week specimens were similar to the 12-week specimens, except that the condyle had attained a nearly normal outline (Fig. 7, B) . The 24-week specimens revealed normal-appearing condyles covered with fibrous conncctivc tissue, bcncath which was a layor 01 hyaline cartilage. HEMICONDYLOIDECTOlZY WITH CONTRALATERAL GRAFT ( IWi. 1) . The 4-week
0.s.. O..\l. L 0.1’. ol~tolwr. 1963
Fig. 7. Fig. 8. l3.q. 7. A, Photomicrograph of a 4-week specimen from an anima,l which untlei~w~~ut a condyloidectomy and graft (Group IIa). Note the bony union of the graft to the condyla~ neck (CA), the active endochondral bone growth in the graft (b)! and the intramembranons bone formation on the medial surface (c). (Hematoxylin and eosm stain. Magnification, x6 ; reduced sh.) I;, Photomicrograph of I&week specimen from Group TIa showing a relatively normal condyle. Note that endochondral bone formation is continuing on the regeneratitrg surface (arrow), while little bone formation is occurring on the grafted side. (Hcmatosylin and eosin stain. Magnification, x6; reduced 15.1 Fig. 8. A, Photomicrograph of a 12.week specimen from Group Tla showing nearly complete regeneration of the condylar outline due to intramembranous bone formation on thcl resected, ungrafted side (arrow). (Hematoxylin and eosin stain. Magnification, x6; r&net1 sj.) I?, High-power photomicrograph of the regenerating area in .4 showing cartilage differentiating in the connective tissue. (Tlcmatoxylin and eosin stain. Magnifiration, x450; reduced :j/5.)
specimen showed bony union between the graft and the normal condyloid process, The articulating surface was covered with fibrous connective tissue which had hyaline cartilage in the deep layer. Endochondral bone formation was occurring in a normal fashion (Fig. 9). The 8-, 12-, and 16-week specimens all resembled normal condylcs (Fig. 10,
Voiume Number
20 4
Pig. 9. Photomicrograph of a 4-week specimen from Group IIb showing bony union of graft (arrow). (Hematoxylin and eosin stain. Magnification, x6; reduced am.) Fig. 10. A, Photomicrograph of a normal adult dog condyle. (Hematoxylin and eosin stain. Magnification, x6; reduced 33.) B, Photomicrograph of a 16-week specimen from Group IIb showing similar condylar outline. There is an increased density of the bone at the site of union of the graft with the mandibular neck (arrow). Note the smooth contour of the articulating surface. (Hematoxylin and eosin stain. Magnification, x6; reduced %.) the
~WILATERAI, CONDYLECTOI~ZT. .411 of tlic specimens showed marked ~‘econstruction of the resected condyle (Fig. 11, A). The surface of the new cond,vle was covered with a fibrous connective tissue layer of varying thickness. No cartilage was present in this layer (Fig. 11, B) . The condyle on the unopera.ted side presented a normal histologic pattern with a thin layer of hyaline cartilage between the fibrous covering and the underlying bone.
Fig. 21. A, Photograph of the regeneration on the operated side graph of specimen from Group III. tissue layer and oondyle (arrows). reduced s/s.)
condyles from a Group III animal illustrating functional (left). (Magnification, x5; reduced ah.) B, PhotomicroNote absence of cartilage cells in zone between connective (Hematoxylin and eosin stain. Magnification, x350;
Volume Number
20 4
Autogenous
codylar
grafts
53 1
DISCUSSION Although these experiments were limited to the mandibular condyle, certain basic concepts which appear to be applicable to bone growth in general can be evolved from the results. For example, it was obvious that, within certain limits, the shape of the growth center is not a crucial factor in determining the ultimate shape of a bone. When a hemicondyloidectomy was performed on the mandible, there was an initial slowing of growth but the shape of the jaw was not affected. Likewise, when the morphology of the condyle was altered by the grafting procedure, no change was noted in the configuration of the mandible. There are two possible explanations, either or both of which may account for these observations. One consideration is the fact that the epiphysis is the widest portion of a bone. This means that during longitudinal growth there is always a gradual reduction in width.7s lo, 3o A s 1ong as the dimensions of the epiphysis are not diminished to less than the diameter of the diaphysis (condylar neck in the mandible), no change in shape may be expected. An alternative explanation can be based upon the fact that the prime function of the epiphysis is to direct longitudinal growth and that bone morphology, while genetically determined, is functionally maintained through the processes of apposition and resorption. Thus, as long as there is an adequate amount of cartilage remaining to continue gr0wt.h and as long as function is maintained, no significant morphologic alterations will occur. Changing the size of an epiphysis has a marked effect upon bone growth. Thus, when half the condyle was resected, there was an initial reduction in the length of the mandible on the operated side. As regeneration of the condyle occurred, this difference gradually diminished until ultimately the jaw again regained its symmetry. It would appear, therefore, that. there is a direct relationship between the size of the growth center in a given bone and the amount of longitudinal growth that occurs. Similar findings have been reported by Westines3 after partial resection of the costochondral junction in rabbits. The results of these experiments emphasize an important difference between the roles of cartilage and connective tissue or periosteum in skeletal growth. During the period that intramembranous bone formation was contributing to reconstruct,ion of the condyle, mandibular growth remained retarded. Not until cartilage re-formed did growth of the mandible begin to attain a more normal rate. These findings support the contention that only cartilage can initiate longitudinal growth, whereas appositional and intramembranous bone formation merely produce local changes in shape during functional reconstruction. The findings in this study distinctly delineate the difference between functional reconstruction and true regeneration of the mandibular eondyle. After condylectomy, a nearly normal shape is attained (Fig. 11, A) and functional mandibular movement returns, but longitudinal mandibular growth remains retarded since the condyIar cartilage does not re-form.23 On the other hand, after henzicondyloidectomy complete regeneration (including regeneration of the cartilage) occurs and normal mandibular growth is reinstituted. A possible explanation for this difference can be found in the st.udies by Weiss31 who noted certain prerequisites for regeneration of organs. These included a stimulus
to provoke formative activity, sufficient; cellular matcri;tI, functional activity. and an adequate supply of food and other vital necessities. Since all the other factors except an inductive stimulus were present in both groups, it may be that the remaining portion of the condylc provides the impetus for rcgenoration of the normal structure.“” This could also explain whys Xarnat?” found only functional reconstruction after removal of the condyle, while Walker’” and Cooper,* who merely dislocated the condyle medially, found complete regeneration. The influence of the recipient site upon the ultimate fate of an epiphyscal bone graft was clearly shown in this investigation. While the portions of the condyle transplanted to the contralateral temporomandibular joint survived the procedure and continued to participate in endochondral bone formation, those inserted in the abdominal wall quickly underwent resorption. It is unlikely that there was a great difference between the nutritional supply in the two areas. If anything, one might expect it to have been better in the subcutaneous region. Rather, it is more logical to assume that the major difference was the degree of function to which the tissue was subjected at. each site. As with other types of bone grafts, normal functional activity may be one of the most important factors in determining the success with which the tissue can be transplanted. When transplanting the hemicondyles, the graft was rotated 180 degrees in order to appose the cut surfaces and maintain a condylar shape that was as nearly normal as possible. However, this rotation did not affect the direction or amount of mandibular growth. In fact, the only deformity was an occasional irregularity in the articular surface. As shown by Brucke,” the essential factor in maintaining proper growth is orientation of the proliferating cartilage columns in the direction of the diaphysis. This, of course, was not changed despite the rotation procedure and therefore growth continued normally. Because of the design of this experiment, the mode of growth of the dog’s mandible could be studied. As in man, the condylar growth center is the main contributor to the over-all length of the jaw. When this growth center was destroyed, the jaw was considerably shortened. On the other hand, growth in the other areas continued. Appositional bone formation occurred on the alveolar process and the body of the mandible. Unlike the human mandible, however, the height and width of the ramus seemed to be controlled by the growth center at the coronoid process, since condylectomy did not affect these measurements. In the dog this growth center persists until maturity, while in the human being it disappears after birth. There are a number of interesting clinical applications for the results of these experiments. Since it has been shown that a transplanted portion of a condyle can be used to maintain mandibular growth, such a procedure may be feasible in patients with a unilateral growth arrest of congenital, traumatic, or inflammatory origin. In such cases, half the normal condylc could be grafted to the affected side. If regeneration of a complete condyle would then occur bilaterally, as was seen in these experiments, only minimal retardation would be expected on the normal side and a considerable recovery of growt.11 would occur on the side of pathologic involvement. Such a surgical restoration appears to be
Volume Number
20 4
Autogenous
c0ndylw
grafts
533
better adapted to the physiologic needs of the area than the use of such distant tissues as the metatarsal or the rib. Another application might be found in young persons who give indications of developing prognathic mandibles. By removing portions of the eondyles at the proper time during the growth period, sufficient retardation may be achieved to maintain a nearly normal jaw relationship. This would then allow the occlusion to be corrected orthodontically rather than surgically. Before such procedures become feasible, however, more information is needed with regard to the prediction of mandibular growth rates. SUMMARY
AND CONCLUSIONS
Thirty-one young dogs were used to study the effects of condylectomy and hemicondyloidectomy, as well as replacement of the resected portions of the condyloid process with autogenous grafts. As a result of both gross and histologic observations, it was concluded that removal of the entire condyle markedly retards growth of the dog mandible and causes some change in shape. Resection of part of the condyloid process, on the other hand, initially reduces the amount of mandibular growth but ultimately the condyle regenerates and relatively normal growth is attained. When an autogenous graft of part of the contralateral side is used to replace the entire condyloid process or a resected half, the graft is able to contribute to mandibular growth and a relatively normal mandible is also achieved. The clinical applications of these findings are discussed. REFERENCES
1. Axhausen, G.: tjber den Histologischen Vorgang bie der Transplantationfahigheit von Gelenkknorpel and Epiphysenknorpel, Arch. klin. Chir. 99: 1, 1912. 2. Bisgard, J. D.: Transplanted Epiphyseal Cartilage, Arch. Surg. 39: 1028, 1939. 3. Brucke, F.: Zur Frage der Bedsutung des Epiphysen Fugenknorpels fur das Wachstum der Langen Rohrenknoeken (Experimentalle Untersuchung iiber Ruckelinplanzung des urn 180” Gedrehte Fugenknorpels), Virchows Arch. path. Anat. 279: 641-670, 1931. 4. Cooper, W.: Personal Communication. Reimplantation des Resecirten intermediarknorpels beim Kaninchen, 5. Enderlen : Zur Deutsche Ztsehr. Chir. 51: 574, 1899. 6. Engel, M. B., and Brodie, A. G.: Condylar Growth and Mandibular Deformities, Surgery ‘22: 976-992, 1947. 7. Enlow. D. H.: Principles of Bone Remodeling, Springfield, ill., 1963, (YI:LI.IPS C Thomas, Publisher, p. 31. 8. Entin, M. : Reconstruction in Congenital Deformity of the Temporomandihular Component, Plast. & Reconstruct. Surg. 21: 461-469, 1958. 9. Fohl, T.: Wersuche iiber die Transplantation der Knorpelfuge, Arrh. klin. Chir. 155: 232, 1929. 10. Haas, 8. L.: The Experimental Transplantation of the Epiphysis With Observations on the Longitudinal Growth of Bones, J. A. M. A. 65: 1965, 1915. 11. Haas, S. L.: Further Observations on the Transplantation of the Epiphyseal Cartilage Plate, Surg. Gynec. 8% Obst. 52: 950, 1931b. 12. Helferich, G. : Versuche iiber die Transplantation des Tntermediarknorpels Waehsender Rohrenknochen, Deutsche Ztschr. Chir. 51: 564, 1899. 13. Herndon, C. II., and Chase, S. W.: Experimental Studies in the Transplantation of Whole *Joints, J. Bone & Joint Surg. 34A: 564578, 1952. 14. Heurlin, R., Gans, B., and Stuteville, 0.: Skeletal Changes Following Fracture Dislocation of the Mandibular Condyle in the Adult Rhesus Monkey, ORAL STJRC.., C&AI. MED. & ORAL PATH. 14: 1490-1500, 1961. 15. Jarabak, J.: Regeneration of the Mandibular Condyle in tho Rat, J. D. Res. 29: 692, 1950. 16. Jarabak, J., and Stuteville, 0.: Bilateral Mandibular Condylar Resection, J. D. Res. 31: 509-510, 1952.
17. 18. 19.
Kazanjian, V. If.: Congenital hbscucc of the Ranrus of III~/ ,\lau~lit~lq ,\IIJ. ,I. O~.tl~w dontics R- Oral Surg. 26: 175, 1940. Kendrick, G., Cameron, .J., and Matthews, J.: ‘rho Uacaca Ithrsus hIonli~~y Skull arId Surgical Intervention, Am. J. Orthodontics 48: 34-44, 1962. Lacroix, P.: The Organization of Bones, T’hiladclphia, 1931, The lilaltiston (k)mpa71~: pp.
12-29.
20. Hehn, E., and Wakabayashi: Die Homoplastische l’ransplant,:ttion dcs 1 tltclnic~tii:?l~lc~~~~~~)~~ls in1 Thiercxperiment, Arch. klin. Chir. 97: I, 1912. 21. Roy, E., and Sarnat, R. G.: Growth Rates of Costochondral Junctions; I'ossiblc ~lpplication to Buman Disease, Transplant. Bull. 3: 80-81, 1956. 22. Sarnat, R. G., and Engel, M. B.: A Serial Study of Maudibular Growth After Removal of the Condyle in the -\Zacaca Rhesus Monkey, Plast. & Rwonstruct. Surg. 7: 364-3i9, 1951. 23. Sarnat, B. G.: Facial and Xruroeranial Growth After Removal of the Mandibular Condyle in the Macaca Rhesus Monkey, Am. J. Surg. 94: 19-30, 1957. 24. Sicher, H. : Oral anatomy, ed. 3, St. Louis, 1960, The C. V. Mosby Company, pp. 117-123. 25. Sichcr, H.: The Growth of the Mandible, J. Periodont. 16: 87-92, 1945. 26. Straub, G.: Anatomical Survival, Growth and Physiological Function of an Epiphyscal Bone Transplant, Surg. Gynnc. & Obst. 48: 687-690, 19%. 27. Stutcville, O., and Lanfranchi, R. : Surgical Xeconstruetion u f the Tcrn~)ororna~ldib~llar Joint. Am. J. Sure-. 90: 940-950. 1955. 28. Uristi RI. R., andQMcLean, F. ‘C.: Osteogenctie Potency and New Bone F’orrnation by Induction in Transplants to the Anterior Chamber of the E.vc, J. Boric S; Joint Surg. 34A: 443-470, 1952: 29. Walker. R. : Traumatic Mandibular Condvlar Fracture Dislocations: Eftoct ou Groxth in the %faeaca Rhesus Monkey, Am. J. St&g. 100: 850-863, 1960. 30. Weinmann, J., and Sicher, II.: Boric and Bows, cd. 2, St. Louis, 1955, ‘I’hc C. V. Mosby Company, ‘pp.’ 57-111. of Drvelopmmt, New York, 1939. ITonry TIoll & Company, pp. 31. Weiss, P. : Principles 458-462. Wenger, H.: Transplantation of Epiphyseal Cartilage, Arch. Burg. 50: 148, 1945. .Tunction, 3332: Westine, J. R.: Growth and Regeneration Mrchanisms in the Contochorrdral M.S. Thesis, University of Illinois, 1963. M. F. A. : The Transplantation of’ Tissues ant1 Orgw~s, Springfic~ld, ill., 1960, 34. Woodruff, Charles C Thomas, Publisher, pp. 389-397.
D.D.S.,
OF ORAL
DENTISTRY,
AND
UNIVERSITY
OF
and Daniel
M.S.,”
AND
DEPARTMENT
11. La&in,
MAXILLOFACIAL
SURGERY,
OF
COLLEGE
SURGERY,
D.D.S.,
COLLEGE OF
ill.S.,‘*
OF
MEDICINE,
ILLINOIS
T
he mandibular condyle is the most important growth center of the mandible.6p 221-25Through interstitial and appositional growth of cartilage in this area, both the height of the ramus and the over-all length of the jaw are increased. Injury to the condylar growth center, whether congenital, traumatic, or inflammatory, can thus produce marked mandibular deformity. This is USUally characterized by the development of antegonial notching, a short and wide ramus, and a shifting of the mandible to the affected side.F3 ** Although experiments on the restoration of lost mandibular growth have been limited,s, 27 a considerable number of studies have been done on the problem of growth arrest in the long bones. These have included investigations on both animals and human beings. The results of Helferich,l* Rehn and Wakaof bayashi,*O Straub, 26 Herndon and Chase,13 and Fohls indicate the feasibility such surgical procedures as epiphyseal transplantation to restore longitudinal growth. The purpose of this investigation was twofold: (1) to evaluate the amount of growth potential which remains after partial removal of the condyle and (2) to determine whether autogenously transplanted condylar growth centers can restore the growth of the mandible after condyloidectomy. The results, based on gross observations and histologic examination, show that the dog condyle retains a major portion of its growth potential, even after partial resection, and that autogenous condylar grafts can be used to restore mandibular growth. This investigation w&5 supported Health, United States Public Health *Instructor in Oral Surgery. **Professor and Associate Head,
by Research Service. Department
Grant
of Oral
DE-01849,
and
National
Maxillofacial
Institutes
of
Surgery.
517
518 REVIEW
l'cskitr
tr~id l,fldi~~
0,s.. O.Jl. & 0.1'. 0~~101 wr,
1!Mz
OF THE LITERATURE
Allh0llgh tll~ tfl’c~c*ts01’mantlih~llat~ Il(~llii~orti~~IectoH1~. II;LVC:1101IKY~IIst uclicd, thta roslllts ot’ ct~I~tlylect.tmky hrvr bcrn cd~m3iwly invcstigatd in both animals ELIlclIklall. Nngcl and Krotlic” noted that in human subjects loss of the condylar groWtl1 Celltrr rcsult,ed in ~IltPg()rli;ll not~hirlg, shiftin, w of the nrandiltle to the affected side, fullness of the face, a,nd development of a short and wide ramux. In animal expcrirnents, Sarnat and ISr~gel~~evaluated tht: results of condylectomy in monkeys. Their findings were comparable to those seen in human bcings. Jarabak15 observed grossly that various amounts of regeneration occurred after condylectomy in young rats, with little or no deformity. Kcndrick, Carncron, and Matthews” removed small sections of the postcrosnpcrior ramal surface, including part of the condyle, in monkeys, Sinccl this procedure included only a vcrp small part of tht : growth center, no effect on growth was noted. In experiments in which the condyles were fractured and dislocated, thus eliminating their contribution to growth. Walker,‘!’ using young monkeys, found regeneration of t,he cond.vlc with only slight growth disturbance. His obsrrvat,ions were based on gross and histologic examination. Jarabak and Stuteville,‘” using a young monkey, obscrvc>dan antcriorlp opened bite and antegonial not.ching, but they also found no appreciable changes in facial growth. Heurlin, Gans, and Stutevillc’” found that, mhcn this same procedure was performed on older monkeys, marked deformities were produced. Thcsc included a decrease in total facial height and a shifting of the mandible to the affected side. The first cxpcrimental attempt, at determining the possibility ot transplanting growth cartilage was made by Helferich,‘2 who cstiscd and reimplanted the lower cpiphysis of the ulna in rabbits. His results showed retention of the property for producing longitudinal growth. .Endcrlcn” made microsco’pic sections of Hclferich’s preparat,ions and found that, the epiphyseal region retained its vit,alitp to a large cxtcnt. In 1912, aftcxr Axhausenl showed that epiphyseal cartilage with its pcrichondrium could survive transplantation, R,ehn and Wakabayashi’” transplanted the head of the radius in rabbits and showed that, it maintained its histologic structure and it,s capacity for longitudinal growth. Fohl” likewise transplanted epiphyseal cartilage in rabbits with excellent rcsult,s. More recently, Herndon and Chase,‘” after a series of homogenous and autogenous joint transplants in dogs, concluded that nutogcnous grafts of epiphyseal cartilage survive while l~omogcnousgrafts are completely resorbed. Contrary to t,he preceding reports, Haas’O reported in 1915 that transplantrd epiphysrs did not contribute to longitudinal growth o-f bones. He repeated his work in 1931’l and confirmed his previous results. Kisgard2 removed sections of the tibia in goat,s and autogcnously transplanted epiphyses to the area. Since no new growth occurred, hc was also opposed to the procedure of’ c$physeal transplantation. Woodruff,“’ after HII extensive review of the subject, concluded that re-establishment of growth in a bone by autotransplantation of a growth center has met with varying results but that, since some successful caseshave been reported, this should stimulate further investigation into the subject. After Fohl” encouraged the transplantation of epiphyseal cartilage in man on the basis of his and other animal expcrimcnts, some clinical cases began to
bc reported. In 1912 StrautP grafted an epiphysis and diaphysis to compcnsatc for loss of the tibia1 cpiphysis from osteomyelitis. The patient was 61/z years old at the time of the surgical procedure. On the basis of gross and radiographic examination made 17 years later, the graft appeared to have survived and growth had proceeded in a normal manner. JVengcr,“” in 1945, reported a case in which he transplanted the cpiphysis and part of the diaphysis of the fibula to the first metatarsal in a 7-year-old patient. The deformity was torrectcd, and the transplant functioned physiologically. Bttempts at correction of the disfiguration caused by loss of the growth center in the mandibular condyle have been mainly in the realm of esthetic reconstruction rather than restoration of growth. Kazanjianl’ used a tibia1 bone graft and advised this method for older patients in whom no growth could be expected. Roy and SarnaP suggested the use of costochondral junction grafts in young patients, with the idea of growth occurring from the graft. No clinical cases in which this method has been used have been reported. Stutevillc and Lanfranchi*’ used the proximal third of the metatarsal in a young girl to replace a hppertrophied condyle. The function of the jaw improved immediately, but the growth aspect of the treatment was not evaluated. Entin* used the metatarsal-pha.langeal joint attached to the mastoid process and the mandible in a case of aplasia of the condyle and ramus. Esthetics were improved but no growth occurred. Up to the present time, there have been no reports of either clinical or experimental studies in which autogenous mandibular condyle grafts were used to restore growth of the mandible. MATERlAL
AND METHODS
Thirty-one dolichocephalic puppies, weighing between 4 and 13 pounds each, were used in this study. Their ages, as determined from the dentition, ranged from 6 to 12 weeks. Each dog was given an intramuscular injection of 300,000 units of benzathine penicillin 2 days preoperatively. At the time of the surgical procedures, the animals were anesthetized with intravenous pentobarbitd sodium. Both sides of the face were shaved, washed with hexachlorophene soap and sterile water, and rinsed with 1:750 benzalkonium chloride. The surgical approach to the temporomandibular joint was the same in each dog. A vertical skin incision was made over the mandibular ramus, extending from just above the zygomatic arch to the inferior border of the mandible. The underlying masseter muscle was separated, exposing the joint capsule. This was incised vertically and the margins were retracted, revealing the articular disc. The attachment, of the disc to the outer aspect of the condyle was then cut to allow lateral dislocation of the mandible. Three types of operation were performed. In Group I (thirteen animals) the lateral half of the condyloid process was removed unilaterally (hemicondyloidectomy) (Fig. 1) _ A No. 700 bur in a dental handpiece was used for this procedure. On the opposite side, a sham operation was performed; a similar approach was made to the temporomandibular joint, but no resection was done. The resected portion of the condyloid process was implanted in a subcutaneous pocket prepared in the anterior abdominal wall.
Group I:
Group II:
Fig. 1. The surgica1 procedures performed on animals in Groups I and II. the color of the graft indicates its original source. Note that the transplantation requires that the grafted portion of the condyle be rotated 180 degrees.
In
Group II procedure
In Group II (twelve animals) the lateral half of the condyloid process was removed bilaterally (Fig. 1). In addition, on one side the medial portion of the condyle was also excised. The resected lateral halves of the condyloid processes were then transplanted to the contralateral sides. They were fixed in position with a transosseous stainless steel wire (0.012 inch in diameber) placed through small bur holes made in the mandibular neck and the transplant (Fig. 1). In Group III (six animals) unilateral condyloidectomy was performed. This served as a control experiment to verify that surgical interference with the condylar growth center of the dog would result in mandibular deformity. Metallic implants were inserted bilaterally into the mandibles of animals in all three groups to provide stable landmarks for direct craniometry. Prior t.o completion of the temporomandibular joint surgery, two small bur holes, one above the other, were made in the bone just inferior to the stump of the condyloid process with a No. 1, round dental bur. A third hole was placed in the body of the mandible near the mental foramina (Fig. 2, A). This was aecomplished through a small incision in the skin and periosteum. After the holes were filled with dental amalgam, the distances between them were measured with a Boley gauge. These measurements were accurate to within 0.1 millimeter. Upon completion of the entire operation, the periosteum and subcutaneous tissues were approximated with 4-O chromic catgut sutures and the skin was
Volume Number
Fig. measured. sured.
dutogenous
20 4
1. A, The positions B, The landmarks
of the metallic used for the
implants mandibular
conclyla~ grafts
placed in the mandible measurements and
521
and the distances the distances mea-
closed with 3-O silk sutures. All incisions were sprayed with a plastic agent (Rezifilm) . Procaine penicillin G, 300,000 units, was administered intramuscularly immediately after the surgical procedure and for 2 days postoperatively. In addition to their normal diet of 50 per cent Purina Dog Chow, 25 per cent Miller’s Puppy Meal, 25 per cent cooked canned horsemeat, and sufficient water to hold the ingredients together, the animals were provided with whole milk for one week postoperatively. Additional drinking water was also provided ad libitum. Two dogs from Groups I and II were killed at intervals of 4, 8, 12, 16, 20, and 24 weeks.* All the animals in Group III were killed after 6 months. After each animal was killed with a lethal dose of pentobarbital sodium, injected intracardially, the head was removed, skinned, and placed in 30 per cent formalin. *A single dog in Group craniometric analysis.
I was also
killed
at 2 weeks.
This
animal
was not
included
in the
Following fixation, the amalgam nii~ik~rs wcr~~ esposc~l illltl cliroc4 tll(~iisI11’+ ments were made bttwcon t hc markers. An addit ional group of int’ils1ir(meiits were also made on each msndible bilaterally (Fig. 2, 11) These inc~ludcd the over-all length oi’ the mandibltt as m(2~suretl fi*orn tlio lllost superior point 011 the alveolar prorcss at the symphysis to the most postcbrior point on the: c~ondyl(~ (A) and from this same s,vmph~-s(lalarea to the most posterior l)oint on thl\ angular process (B) ; the height of the bod,v of the mandible as ~~~cw~wt~d from the inferior border to the alveolar margin in the region of the major mental ~OIXITICII (C) ; the height of the ramus as measured from the tip of the coronoid process on a line perpendicular to the inferior border (I)) ; thcl most postcrioia point on the condylc to the posterior margin of the major mental fo~arno~~ (14:) ; the most posterior point on the condylc to the most postrrior point 011the angular process (F) ; the tip of the coronoid process to the most posterior point on the condylc (G) ; the anterior border of the ramus to the posterior border of the ramus at the level of the most posterior point on the c~~nd~la (II) ; the posterior border of the ramus to the most posterior point on the cond,vlc (I) ; and the posterior margin of the major mental foramcn to the most superiol point on the alveolar process at the symphgsis (J). For the histologic aspect, of t,he stud,v, the condyloid process and the SUP rounding tissues were excisrd from the skull en bloc by means of a. coping saw, mallet, and chisel. The specimens were decalcified in a solution containing equal parts of 50 per cent formic acid and 20 per cent sodium citrate. When radiographs showed that the bone was decalcified, the specimens wcrc washed, tlchydrated, and infiltra.ted with crlloidin. Serial sections wcrc stained with llenliltoxylin and eosin and mounted on slides with synthetic mountinK rcGn ant1 XJkllP.
RESULTS Gross
observations
All of the animals were examined 4 days postoperatively, and it, was found that two dogs in Group I had some purulent drainage from the preauricular incisions. One week postoperatively, however, when the skin sutures were rcmoved, none of the animals showed any evidence of infection and all incisions were clinically healed. The dogs generally exhibited moderate edema and limitation of mandibular function for the first 2 weeks. In the animals killed between 2 and 4 weeks, this limitation was evidenced by the presence of gross calcareous deposits on the teeth. In the animals subsequently killed, only slight amounts of calculus were found. After the second week food consumption began to increase and mandibular function improved. By the third to the fourth week, the animals again began to gain weight. Mandibular function appeared normal at that t,ime. On exploration of t,he abdominal area at the time of death of the CY’OLI~ I dogs, none of the tr.a,nsplantetl portions of the condgle were found, although healing of the incisions appeared normal. It was thought that, the transplants had been resorbed since only a fibrous mass remained. No grossly visible changes in the shape of the mandible were noted at any
Autogenous
co~~dylnr
grafts
523
time in dogs of either Group I or II. ROWC~C~,some minor oeclusal irrcgularities were observed. In the 4-, 8-, and 12-week specimens of Group I, the mandible had shifted somewhat to the side of the hemicondyloidectomy. The mandibular teeth on the unoperated side were slightly lingual t,o their normal position in relation to the maxillary teeth. This deformity was not present in the 16-, 20-, and 24-week specimens. The 4-, 8-, and E-week specimens in Group II displayed the same deformity as seen in Group I, with a shift of the mandible to the side of the condyloideetomy and contralateral graft. This was not observed in the older animals. In Group III all of the animals showed a marked shift of the mandible to the side of the condylectomy. The posterior teeth remained in occlusion, but in the incisor region the midline of the mandible was skewed to the operated side (Fig. 3). Some gross changes in the shape of the mandible were noted in this group. The depth of the notch anterior to the angular process was increased on the operated side. Likewise, the height and thickness of the body of the mandible were increased. Craniometry
Most of the metallic implants in the animals killed between 4 and 12 weeks remained in the bone and maintained the samepositions as at the time of surgical intervention. In the animals killed between 16 and 24 weeks, however, the posterior markers were frequently found in the masseter muscle. This was a result of growth and remodeling of the ramus. In these instances measurements could not be made. In Group I the 4-, 8-, and 12-week specimens showed a slight underdevelopment of the mandible on the side of the hemicondyloidectomy. The over-all length as measured from the condyle to the symphysis was always less than on the control side (Table I). The distance from the angular process to the symphysis was also less, as was the measurement from the condyle to the angular process. The height of the coronoid process and the width of the ramus, how-
Note
Fig. 3. The relationship of t,he anterior teeth the shift of the mandible to the operated
at the time side.
of death
in a Group
111
animal.
-______
._ l’ime
Dog
after surgery (weeks)
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l)ifl’wenr:cs
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T/J
:
: 3
4 i
2.7 2.9 2.1
2.2 2.4 1.2
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2.0 0.4 0.5 -0.1 -0.4
if -0:s -0.1 0.1
-0.2 0.2 -0.4 -0.6 0.2
2.2 0.9 0.4 0.6 0.3
1.1 0.7 0.9 -0.5 -0.4
-0.1 0.1 -0.3 -0.1 0.3
-0.4 0.: -0.1 0.3
-;+ -0:” 0.3 0.2
-0.2 0.1 0.2 -0.2 0.1
9 10
20 20
0.3 -1.1
-0.4 0.6
0.1 0.1
0 0.7
-1.0 0.8
0.4 -0.4
-:*y
0.2 -0.3
--0.9 0“
0 n
11 12 -0.2 0.3 -0.3 0.2 -0.4 0.3 -0.40 0:2 -0.2 -0.6 -0:; 24 0.7 -0.5 0.1 -0.1 0.3 0. 1. -0.:’ *All numbers are expressed in millimeters and are accurate to 1 0.1. A negative value indicates that the distance on the control side was less than that on the side of the hemicondyloidectomy. The letters correspond with those shown in Fig. 2, R and indicate the f ollorving measurements : F = Condyle to angular process. A = Condyle to symphysis. 13 = Angular process to symphysis. G z Condyle to coronoid process. C = Height of body of mandible. H z Width of ramus. D = Height of ramus. I z Condyle to anterior ramus. E = Condyle to mental foramen. J = Mental foramen to symphysis.
ever, were not affected by the hemicondyloidectomy. Likewise, as indicated by the random distribution of the differences, the height of the body of the mandible was not changed by this procedure. These changes were not observed in the 16-, 20-, and 24-week specimens. In the Group II animals killed between 4 and 12 weeks, the changes in size noted when side A (condyloidectomy and contralateral graft) was compared with side B (hemicondyloidectomy and contralateral graft) were relatively similar to those seen when the operated and control sides were compared in the young Group I animals (Table II). No significant differences between sides A and B were observed in the 16-, 20-, and 24-week specimens. The Group III animals showed a marked retardation of growth on the side of the condylectomy. The over-all length of the jaw was markedly reduced. On the other hand, the height of the body of the mandible was greater on the operated side when compared to the control. The only measurements that wcrc not affected were those on the coronoid process (Table III). Histologic
observations
Group I. The a-week specimen showed the site of the hemicondyloidectomy to be healing normally. Young fibrous connective tissue was beginning to proliferate over the cut surface of the condyle (Fig. 4). By the end of 4 weeks, this area was completely covered with a layer of fibrous connective tissue. Some membranous bone formation was occurring in the deepest part of this layer. Active differentiation of cartilage cells and endochondral bone growth were continuing in the unoperated portion of the condyle (Fig. 5, A).
Volume Number
20 4
flut0,genou.s
condylar
525
grafts
Table II. Comparison of measurements on the side of hemicondyloidectomy graft with those on the side of condyloidectomy and graft (Group II)
nnO
!Eme after surgery , (weeks)
Differences 2.1
1.5
2.9
3.1 1.1
2.0 1.8
1.1 1.4 0.6 -0.4 0.8
16 76
io
20 24 24
12
measwements*
A\BJCIDJEjFlGIHl
4 4 8 8
7 8 9 10 11
between
2.6 1.2 1.7 -0.6 -0.2
-0.1
-1.0 4.2
0.7 -0.9
0.3 0.9
and
I\J -0.1 0 0.8 0.1 -0.1
1.0
-0.9 0.2
1.7 2.2 1.8
1.0 1.8 1.1
--0.1 0.7 --0.3
0.3
2.1
1.1
0.4
0.3
0.9
0.4
0
-0.1
-0.2 -0.2 0.2
-0.3 0.7 0.9
o".: -0:4
--0.1 --0.1
0 -0.2
-0.4
0.1
-0.1 0 -0.1
-0.6 0 0.2
f$ -0:2 0.4
0
0.3
-0.9
0 0.6 -0.2 0.2 0.2
0.4 0.2 0.2 -0.7 0.2
0.8 -0.4
-0.8
1.0 -2.1 0.1 0.2 0.2
0.7
-0.1 0
1.0
1.8
0.5 -0.2
-0.1
;.,”
-0.3 0.2
0.1 0.8
-0:3
-0.2
0
0 0.3
-0.2 -0.4
0.1 0
0.1
*All numbers are expressed in millimeters and are accurate to 20.1. A negative value indicates that the distance on the side of the hemicondyloidectomy and graft was less than that on the side of the condyloidectomy and graft. The letters correspond with those shown in Fig. 2, B and indicate the following measurements: F = Condyle to angular process. A = Condyle to symphysis. B = Angu!ar process to symphysis. G = Condyle to coronoid process. C = Height of body of mandible. H = Width of ramus. I = Condyle to anterior ramus. D = Height of ramus. E = Condyle to mental foramen. J = Mental foramen to symphysis.
Table Ill. Comparison of measurements on the control side with those on the side of the condyloidectomy (Group III) I Dog 1
I
A
1
B
)
C
Diferences 1 D
j
between, E 1
meaSUTementS*
F
I
G
1
H
I
1
1
J
32
7.2 4.2 7.9
8.1 6.7 3.8
3.9 2.7 4.3
0.1 -0.1 0.7
4.2 4.3 3.4
2.5 4.7
-0.3 0 3 0.5
0.3 -0.90.2
7.9 w3
0.2 0.3
z 6
7.5 ifi::
67 7.2 7:3
4.8 5.1 4.6
-0.30.7 -0.3
$4 3:8
4';i 7 3:4
0'34 1:2
-0.40.7 -0.4
4'2 5:l 8.2
0:s o".i 0.4
*All numbers are expressed in millimeters and are accurate indicates that the distance on the control side was less than dyloidectomy. The letters correspond with those shown in Fig. ing measurements : A = Condyle to symphysis. F = Condyle B = Angu’ar process to symphysis. G = Condyle C = Height of body of mandible. H = Width D = Height, of ramus. I = Condyle E = Condyle to mental foramen. J = Mental
to kO.1. A negative value that on the side of the con2, B and indicate the followto angular process. to eoronoid process. of ramus. to anterior ramus. foramen to symphysis.
The a-week specimens were very similar to those from the d-week group. However, between 8 and 12 weeks there was a great increase in membranous bone formation in the resected area. This new bone formation had resulted in the condylc attaining a. relatively normal outline. The entire articulat,ing surface was covcrcd with mature fibrous conne&ive tissue. However, hyaline rartilagc st,iIl had not re-formed in the deepest layer of the operated side (Fig. 5, B) . In the 16- and 20-week specimens the rescctcd portion of the condyle had
0.5.. 0.11.
1'Hi.i
undergone almost complete regeneration. The lateral port.ion now contained some cartilage cells in the deep layer (Fig. 6, A and B). Fndochondral boric growth was actively occurring. The 24week specimens showed well-formed condyles of the adult type. The surface was covered with a thin fibrous connectivc tissue lqvcr, hencath which was a narrow cartilage laycxr of uniform thickness. There was no longer any significa.nt dcgrec of cndochondral boric formation in thcsc spccimc~ns. CONDYLOIDECTOillY
WITH
CONTR,ZLATERAL
mens bony union had occurred
between
GRAFT
the graft
I). In the I-week speciand the mandibular n~k. The (FIG.
Volurrlr~ Number
20 a
ilutogenous
co,~dylar
grafts
527
Fig. 6. A, Photomicrograph of a 16-~~-eek specimen showing complete regeneration of the structure. (Hematoxylin and eosin stain. Magnification, x6; reclucecl 3h.) B, High-power photomicrograph of the outlined area in A showing cartilage cells in the deep layer of the fibrous connective tissue. (Hematoxylin and eosin stain. Magnification, x350; reduced T/i.)
graft was properly oriented and showed evidence of partieipat.ion in endochondral bone growth. A thin fibrous connective tissue layer covered the area where the medial aspect of the condyle had been excised (Fig. 7, A). This specimen closely resembled the 4-week specimen of Group I. In the EL and 12-week specimens the condyle had a nearly normal outline. This was due to membranous bone formation which had occurred within the fibrous connective tissue in the resected a.rea. There were now some cartilage cells in this layer (Fig. 8, A and 13). The 16- and 20-week specimens were similar to the 12-week specimens, except that the condyle had attained a nearly normal outline (Fig. 7, B) . The 24-week specimens revealed normal-appearing condyles covered with fibrous conncctivc tissue, bcncath which was a layor 01 hyaline cartilage. HEMICONDYLOIDECTOlZY WITH CONTRALATERAL GRAFT ( IWi. 1) . The 4-week
0.s.. O..\l. L 0.1’. ol~tolwr. 1963
Fig. 7. Fig. 8. l3.q. 7. A, Photomicrograph of a 4-week specimen from an anima,l which untlei~w~~ut a condyloidectomy and graft (Group IIa). Note the bony union of the graft to the condyla~ neck (CA), the active endochondral bone growth in the graft (b)! and the intramembranons bone formation on the medial surface (c). (Hematoxylin and eosm stain. Magnification, x6 ; reduced sh.) I;, Photomicrograph of I&week specimen from Group TIa showing a relatively normal condyle. Note that endochondral bone formation is continuing on the regeneratitrg surface (arrow), while little bone formation is occurring on the grafted side. (Hcmatosylin and eosin stain. Magnification, x6; reduced 15.1 Fig. 8. A, Photomicrograph of a 12.week specimen from Group Tla showing nearly complete regeneration of the condylar outline due to intramembranous bone formation on thcl resected, ungrafted side (arrow). (Hematoxylin and eosin stain. Magnification, x6; r&net1 sj.) I?, High-power photomicrograph of the regenerating area in .4 showing cartilage differentiating in the connective tissue. (Tlcmatoxylin and eosin stain. Magnifiration, x450; reduced :j/5.)
specimen showed bony union between the graft and the normal condyloid process, The articulating surface was covered with fibrous connective tissue which had hyaline cartilage in the deep layer. Endochondral bone formation was occurring in a normal fashion (Fig. 9). The 8-, 12-, and 16-week specimens all resembled normal condylcs (Fig. 10,
Voiume Number
20 4
Pig. 9. Photomicrograph of a 4-week specimen from Group IIb showing bony union of graft (arrow). (Hematoxylin and eosin stain. Magnification, x6; reduced am.) Fig. 10. A, Photomicrograph of a normal adult dog condyle. (Hematoxylin and eosin stain. Magnification, x6; reduced 33.) B, Photomicrograph of a 16-week specimen from Group IIb showing similar condylar outline. There is an increased density of the bone at the site of union of the graft with the mandibular neck (arrow). Note the smooth contour of the articulating surface. (Hematoxylin and eosin stain. Magnification, x6; reduced %.) the
~WILATERAI, CONDYLECTOI~ZT. .411 of tlic specimens showed marked ~‘econstruction of the resected condyle (Fig. 11, A). The surface of the new cond,vle was covered with a fibrous connective tissue layer of varying thickness. No cartilage was present in this layer (Fig. 11, B) . The condyle on the unopera.ted side presented a normal histologic pattern with a thin layer of hyaline cartilage between the fibrous covering and the underlying bone.
Fig. 21. A, Photograph of the regeneration on the operated side graph of specimen from Group III. tissue layer and oondyle (arrows). reduced s/s.)
condyles from a Group III animal illustrating functional (left). (Magnification, x5; reduced ah.) B, PhotomicroNote absence of cartilage cells in zone between connective (Hematoxylin and eosin stain. Magnification, x350;
Volume Number
20 4
Autogenous
codylar
grafts
53 1
DISCUSSION Although these experiments were limited to the mandibular condyle, certain basic concepts which appear to be applicable to bone growth in general can be evolved from the results. For example, it was obvious that, within certain limits, the shape of the growth center is not a crucial factor in determining the ultimate shape of a bone. When a hemicondyloidectomy was performed on the mandible, there was an initial slowing of growth but the shape of the jaw was not affected. Likewise, when the morphology of the condyle was altered by the grafting procedure, no change was noted in the configuration of the mandible. There are two possible explanations, either or both of which may account for these observations. One consideration is the fact that the epiphysis is the widest portion of a bone. This means that during longitudinal growth there is always a gradual reduction in width.7s lo, 3o A s 1ong as the dimensions of the epiphysis are not diminished to less than the diameter of the diaphysis (condylar neck in the mandible), no change in shape may be expected. An alternative explanation can be based upon the fact that the prime function of the epiphysis is to direct longitudinal growth and that bone morphology, while genetically determined, is functionally maintained through the processes of apposition and resorption. Thus, as long as there is an adequate amount of cartilage remaining to continue gr0wt.h and as long as function is maintained, no significant morphologic alterations will occur. Changing the size of an epiphysis has a marked effect upon bone growth. Thus, when half the condyle was resected, there was an initial reduction in the length of the mandible on the operated side. As regeneration of the condyle occurred, this difference gradually diminished until ultimately the jaw again regained its symmetry. It would appear, therefore, that. there is a direct relationship between the size of the growth center in a given bone and the amount of longitudinal growth that occurs. Similar findings have been reported by Westines3 after partial resection of the costochondral junction in rabbits. The results of these experiments emphasize an important difference between the roles of cartilage and connective tissue or periosteum in skeletal growth. During the period that intramembranous bone formation was contributing to reconstruct,ion of the condyle, mandibular growth remained retarded. Not until cartilage re-formed did growth of the mandible begin to attain a more normal rate. These findings support the contention that only cartilage can initiate longitudinal growth, whereas appositional and intramembranous bone formation merely produce local changes in shape during functional reconstruction. The findings in this study distinctly delineate the difference between functional reconstruction and true regeneration of the mandibular eondyle. After condylectomy, a nearly normal shape is attained (Fig. 11, A) and functional mandibular movement returns, but longitudinal mandibular growth remains retarded since the condyIar cartilage does not re-form.23 On the other hand, after henzicondyloidectomy complete regeneration (including regeneration of the cartilage) occurs and normal mandibular growth is reinstituted. A possible explanation for this difference can be found in the st.udies by Weiss31 who noted certain prerequisites for regeneration of organs. These included a stimulus
to provoke formative activity, sufficient; cellular matcri;tI, functional activity. and an adequate supply of food and other vital necessities. Since all the other factors except an inductive stimulus were present in both groups, it may be that the remaining portion of the condylc provides the impetus for rcgenoration of the normal structure.“” This could also explain whys Xarnat?” found only functional reconstruction after removal of the condyle, while Walker’” and Cooper,* who merely dislocated the condyle medially, found complete regeneration. The influence of the recipient site upon the ultimate fate of an epiphyscal bone graft was clearly shown in this investigation. While the portions of the condyle transplanted to the contralateral temporomandibular joint survived the procedure and continued to participate in endochondral bone formation, those inserted in the abdominal wall quickly underwent resorption. It is unlikely that there was a great difference between the nutritional supply in the two areas. If anything, one might expect it to have been better in the subcutaneous region. Rather, it is more logical to assume that the major difference was the degree of function to which the tissue was subjected at. each site. As with other types of bone grafts, normal functional activity may be one of the most important factors in determining the success with which the tissue can be transplanted. When transplanting the hemicondyles, the graft was rotated 180 degrees in order to appose the cut surfaces and maintain a condylar shape that was as nearly normal as possible. However, this rotation did not affect the direction or amount of mandibular growth. In fact, the only deformity was an occasional irregularity in the articular surface. As shown by Brucke,” the essential factor in maintaining proper growth is orientation of the proliferating cartilage columns in the direction of the diaphysis. This, of course, was not changed despite the rotation procedure and therefore growth continued normally. Because of the design of this experiment, the mode of growth of the dog’s mandible could be studied. As in man, the condylar growth center is the main contributor to the over-all length of the jaw. When this growth center was destroyed, the jaw was considerably shortened. On the other hand, growth in the other areas continued. Appositional bone formation occurred on the alveolar process and the body of the mandible. Unlike the human mandible, however, the height and width of the ramus seemed to be controlled by the growth center at the coronoid process, since condylectomy did not affect these measurements. In the dog this growth center persists until maturity, while in the human being it disappears after birth. There are a number of interesting clinical applications for the results of these experiments. Since it has been shown that a transplanted portion of a condyle can be used to maintain mandibular growth, such a procedure may be feasible in patients with a unilateral growth arrest of congenital, traumatic, or inflammatory origin. In such cases, half the normal condylc could be grafted to the affected side. If regeneration of a complete condyle would then occur bilaterally, as was seen in these experiments, only minimal retardation would be expected on the normal side and a considerable recovery of growt.11 would occur on the side of pathologic involvement. Such a surgical restoration appears to be
Volume Number
20 4
Autogenous
c0ndylw
grafts
533
better adapted to the physiologic needs of the area than the use of such distant tissues as the metatarsal or the rib. Another application might be found in young persons who give indications of developing prognathic mandibles. By removing portions of the eondyles at the proper time during the growth period, sufficient retardation may be achieved to maintain a nearly normal jaw relationship. This would then allow the occlusion to be corrected orthodontically rather than surgically. Before such procedures become feasible, however, more information is needed with regard to the prediction of mandibular growth rates. SUMMARY
AND CONCLUSIONS
Thirty-one young dogs were used to study the effects of condylectomy and hemicondyloidectomy, as well as replacement of the resected portions of the condyloid process with autogenous grafts. As a result of both gross and histologic observations, it was concluded that removal of the entire condyle markedly retards growth of the dog mandible and causes some change in shape. Resection of part of the condyloid process, on the other hand, initially reduces the amount of mandibular growth but ultimately the condyle regenerates and relatively normal growth is attained. When an autogenous graft of part of the contralateral side is used to replace the entire condyloid process or a resected half, the graft is able to contribute to mandibular growth and a relatively normal mandible is also achieved. The clinical applications of these findings are discussed. REFERENCES
1. Axhausen, G.: tjber den Histologischen Vorgang bie der Transplantationfahigheit von Gelenkknorpel and Epiphysenknorpel, Arch. klin. Chir. 99: 1, 1912. 2. Bisgard, J. D.: Transplanted Epiphyseal Cartilage, Arch. Surg. 39: 1028, 1939. 3. Brucke, F.: Zur Frage der Bedsutung des Epiphysen Fugenknorpels fur das Wachstum der Langen Rohrenknoeken (Experimentalle Untersuchung iiber Ruckelinplanzung des urn 180” Gedrehte Fugenknorpels), Virchows Arch. path. Anat. 279: 641-670, 1931. 4. Cooper, W.: Personal Communication. Reimplantation des Resecirten intermediarknorpels beim Kaninchen, 5. Enderlen : Zur Deutsche Ztsehr. Chir. 51: 574, 1899. 6. Engel, M. B., and Brodie, A. G.: Condylar Growth and Mandibular Deformities, Surgery ‘22: 976-992, 1947. 7. Enlow. D. H.: Principles of Bone Remodeling, Springfield, ill., 1963, (YI:LI.IPS C Thomas, Publisher, p. 31. 8. Entin, M. : Reconstruction in Congenital Deformity of the Temporomandihular Component, Plast. & Reconstruct. Surg. 21: 461-469, 1958. 9. Fohl, T.: Wersuche iiber die Transplantation der Knorpelfuge, Arrh. klin. Chir. 155: 232, 1929. 10. Haas, 8. L.: The Experimental Transplantation of the Epiphysis With Observations on the Longitudinal Growth of Bones, J. A. M. A. 65: 1965, 1915. 11. Haas, S. L.: Further Observations on the Transplantation of the Epiphyseal Cartilage Plate, Surg. Gynec. 8% Obst. 52: 950, 1931b. 12. Helferich, G. : Versuche iiber die Transplantation des Tntermediarknorpels Waehsender Rohrenknochen, Deutsche Ztschr. Chir. 51: 564, 1899. 13. Herndon, C. II., and Chase, S. W.: Experimental Studies in the Transplantation of Whole *Joints, J. Bone & Joint Surg. 34A: 564578, 1952. 14. Heurlin, R., Gans, B., and Stuteville, 0.: Skeletal Changes Following Fracture Dislocation of the Mandibular Condyle in the Adult Rhesus Monkey, ORAL STJRC.., C&AI. MED. & ORAL PATH. 14: 1490-1500, 1961. 15. Jarabak, J.: Regeneration of the Mandibular Condyle in tho Rat, J. D. Res. 29: 692, 1950. 16. Jarabak, J., and Stuteville, 0.: Bilateral Mandibular Condylar Resection, J. D. Res. 31: 509-510, 1952.
17. 18. 19.
Kazanjian, V. If.: Congenital hbscucc of the Ranrus of III~/ ,\lau~lit~lq ,\IIJ. ,I. O~.tl~w dontics R- Oral Surg. 26: 175, 1940. Kendrick, G., Cameron, .J., and Matthews, J.: ‘rho Uacaca Ithrsus hIonli~~y Skull arId Surgical Intervention, Am. J. Orthodontics 48: 34-44, 1962. Lacroix, P.: The Organization of Bones, T’hiladclphia, 1931, The lilaltiston (k)mpa71~: pp.
12-29.
20. Hehn, E., and Wakabayashi: Die Homoplastische l’ransplant,:ttion dcs 1 tltclnic~tii:?l~lc~~~~~~)~~ls in1 Thiercxperiment, Arch. klin. Chir. 97: I, 1912. 21. Roy, E., and Sarnat, R. G.: Growth Rates of Costochondral Junctions; I'ossiblc ~lpplication to Buman Disease, Transplant. Bull. 3: 80-81, 1956. 22. Sarnat, R. G., and Engel, M. B.: A Serial Study of Maudibular Growth After Removal of the Condyle in the -\Zacaca Rhesus Monkey, Plast. & Rwonstruct. Surg. 7: 364-3i9, 1951. 23. Sarnat, B. G.: Facial and Xruroeranial Growth After Removal of the Mandibular Condyle in the Macaca Rhesus Monkey, Am. J. Surg. 94: 19-30, 1957. 24. Sicher, H. : Oral anatomy, ed. 3, St. Louis, 1960, The C. V. Mosby Company, pp. 117-123. 25. Sichcr, H.: The Growth of the Mandible, J. Periodont. 16: 87-92, 1945. 26. Straub, G.: Anatomical Survival, Growth and Physiological Function of an Epiphyscal Bone Transplant, Surg. Gynnc. & Obst. 48: 687-690, 19%. 27. Stutcville, O., and Lanfranchi, R. : Surgical Xeconstruetion u f the Tcrn~)ororna~ldib~llar Joint. Am. J. Sure-. 90: 940-950. 1955. 28. Uristi RI. R., andQMcLean, F. ‘C.: Osteogenctie Potency and New Bone F’orrnation by Induction in Transplants to the Anterior Chamber of the E.vc, J. Boric S; Joint Surg. 34A: 443-470, 1952: 29. Walker. R. : Traumatic Mandibular Condvlar Fracture Dislocations: Eftoct ou Groxth in the %faeaca Rhesus Monkey, Am. J. St&g. 100: 850-863, 1960. 30. Weinmann, J., and Sicher, II.: Boric and Bows, cd. 2, St. Louis, 1955, ‘I’hc C. V. Mosby Company, ‘pp.’ 57-111. of Drvelopmmt, New York, 1939. ITonry TIoll & Company, pp. 31. Weiss, P. : Principles 458-462. Wenger, H.: Transplantation of Epiphyseal Cartilage, Arch. Burg. 50: 148, 1945. .Tunction, 3332: Westine, J. R.: Growth and Regeneration Mrchanisms in the Contochorrdral M.S. Thesis, University of Illinois, 1963. M. F. A. : The Transplantation of’ Tissues ant1 Orgw~s, Springfic~ld, ill., 1960, 34. Woodruff, Charles C Thomas, Publisher, pp. 389-397.