Effect of Experimental Surgery on Mandibular Growth in Syrian Hamsters

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Effect of Experimental Surgery                        on   Mandibular Growth
in Syrian Hamsters

W. A. CASTELLI, P. C. RAMIREZ, and A. R. BURDI
Department of Anatomy and Center for Human Growth and Development, University of
Michigan, Ann Arbor, Michigan 48104, USA

Enucleation of the incisor germinal center            anterior to the external acoustic meatus,
and extraction of molars in the mandibles             displacing the parotid gland laterally, ex-
of young hamsters produced a significant              posing the outer surface of the masseter
decrease in the size of the mandibular body,          muscle, and separating the masseter fibers
loss of normal occlusion, and a shift of the          that cover the region of the temperoman-
mandibular body medially and cranially.               dibular joint. Ultimate fracturing of the
Condylectomies mainly affected the length             condylar neck was done by use of a thin,
of the mandible and were closely related              bent hemostat; all condyles were removed
to loss of the articular cartilage and impair-        after fracture.
ment of ramal growth.                                    In the second experimental series, enucle-
                                                      ation of the right incisor germinal center
Postnatal mandibular growth1'2 can be im-             and extraction of all right mandibular mo-
paired by abnormal development of the                 lars were done by use of an extraoral
mandibular condyle,3 ankylosis of the tem-            approach. The lateral surface of the body
poromandibular joint,4'5 and by several               of the mandible was exposed through an
pathologic complications6-9 that are often            incision made parallel to the mandibular
treated by partial mandibular resection with          base. With surgical burs, the incisor ger-
loss of teeth or tooth germs. However, the            minal center was located in the bone below
effects of mandibular surgery on the growth           the molar region. Actual enucleation was
and functional morphology of the mandible             accomplished by use of small dental and
still lack adequate explanation in surgical           surgical curettes. Hemorrhage was controlled
literature.                                           by packing the cavity with sterile cotton
    This study is concerned with the effects          pellets. After each enucleation procedure,
of each of the following on mandibular                an intraoral approach was used for the ex-
growth: unilateral condylectomies of the              traction of the three molars and removal
mandible, enucleation of the incisor ger-             of the incisor crown.
minal center, and extraction of molars.                  Sham operations, which consisted of the
Additional attention is given to a compari-           same surgical sequences followed for con-
son of the traumatizing effects of each of            dylectomy and enucleation procedures,
the three surgical procedures.                        were performed on the left side in hamsters
           Material and Methods                       whose right condyles were resected and right
                                                      incisors enucleated. These sham operations
  Thirty-six 3-week-old Syrian hamsters               did not break through the mandibular body
were placed into two experimental groups              but were deep enough to reach it.
of 13 hamsters each and one control group                After six postoperative months, all ham-
of 10 hamsters. Right condylectomies were             sters were killed and decapitated. Each
performed in one experimental series by               head was carefully macerated in a steam
making a vertical skin incision immediately           cooker in preparation for direct measure-
  This study was supported by USPHS Grant 02272 and   ments. All measurements were made with
Grant 1433 from Faculty Research, Horace H. Rackham   calipers, read to the nearest tenth of a milli-
School of Graduate Studies, University of Michigan,   meter, and verified; double-blind determina-
Ann Arbor, Mich.
  Received for publication December 26, 1969.         tions were performed for accuracy.
356
Vol 50 No. 2                             MANDIBULAR GROWTH IN HAMSTERS                    357
                                          TABLE 1
                                  MANDIBULAR MEASUREMENTS
                   Variables                           Description
          Length                      (1) Condylion-infradentale (C-G) (enucleation
                                           and control series);
                                      (2) Supraangular notch-infradentale (N-G)
                                           (condylectomy and control series)
          Ramus width                 Measure taken at most convex point of borders
                                        of coronoid process and angle (P-O) (surgical
                                        and control series)
          Body height                 Alveolar ridge-basilar border (Z-O) (surgical
                                        and control series)
          Medial shift of mandible    Gonion-tympanic bulla (G-B) (surgical and
                                        control series)
          Intermandibular distance    Distance between right and left antegonial notch
                                         (f-M) (surgical and control series)
          Alveolar height             Distance from base of orbit to molar occlusal
            increment (maxilla)         plane (O-M) (enucleation and control series)

   The six variables studied and their de-       appeared to alter little of the typical man-
scriptions are listed in Table 1 and shown       dibular shape. Similarly, there was little
in Figure 1.                                     change in the spatial position of the grow-
   In experimental and control groups,           ing, operated-on hemimandible. In this se-
t tests for difference of means were com-        ries, mandibular length was the only variable
puted for the six variables of the deeply        modified significantly (Table 3, Fig 3).
exposed mandibles and the sham-operated          Experimental sides were shorter (P = 0.01)
hemimandibles. Those dimensions that var-        than the sham-operated sides.
ied significantly in both experimental series       EXPERIMENTAL AND CONTROL HAMSTER
were also t-tested against corresponding     COMPARISONS.-Ten control hamsters were
measurements in the control contralateral    used for testing variables that were signifi-
hemimandibles.                               cantly modified either by condylectomy or
                                             by enucleation-extraction procedures. Left
                   Results                   hemimandibles of control hamsters were
   Gross examination of the specimens re- measured. These corresponded to the sham
vealed a substantial morphologic and spatial sides in the two surgical series. As expected
alteration of the experimental hemiman- by the statistical analysis of these compari-
dibles in the enucleation series. Primary sons (Table 4), there was a highly signifi-
observations were a decrease in size of the cant difference (P = 0.01) for medial shift
mandibular body, a loss of normal occlu- and body height when the hemimandibles
sion, and a shift of the mandibular body of the enucleated series were tested against
medially and cranially. No noticeable the control contralateral sides.
changes in occlusion were present in the        Statistical analyses of the length of the
hamsters with resected right mandibular experimental hemimandibles in the con-
condyles. Regeneration of a pseudo-condyle, dylectomy series and control contralateral
of limited extent, was oberved in the spec- sides (Table 4) gave a highly significant
imens (Figs 2, 3).                           difference as well (P = 0.01).
   ENUCLEATION SERIES.-Since no incisor         The distance between the right and left
reappeared after surgery, enucleation of mandibular bodies also was reduced sig-
right incisor germinal centers in all ham- nificantly as a result of the enucleation-
sters was considered complete. Enucleation extraction procedure (Table 4).
did not alter either the width of the ramus
or the length of the mandible. This opera-                      Discussion
tion, however, was responsible for signifi-     Although incisors constitute a great part
cant changes (P = 0.01) in body height and of the mandibular body in hamsters, the
medial shifting of the experimental hemi- amount of tissue lost because of the enu-
mandibles (Table 2, Fig 2).                  cleation procedure was limited solely to the
   CONDYLECTOMY SERIES.-Condylectomy incisor germinal center and the bone that
358     CASTELLI, RAMIREZ, AND BURDI                            J Dent Res   March-April 1971

                   F1IG 1.-L inear mea-surements (Table 1) used in study.

coverecl it. The aialn bulk of the tooth, Iv-   a rcsuilt of the enuicleatioii-extractioln pro-
ing anterior to the extirpated germinal cen-    cedure. At least three factors seemed to
ter, remained intact in the body of the         contribute to this morphologic distortion:
mandible.                                       (1) the extraction of teeth, which produced
   The most pronounced morphologic              resorption of the alveolar cortex and loss
changes were obtained in the mandibles as       of vertical dimension and normal occlu-
FIG 2.-Macerated skulls show deep morphologic alterations as result of enucleation-extrac-
tion procedure. Medial shifting of operated hemimandible (MS) allowed a significant decrease
in gonion-bulla distance of same side. ADI, maxillary alveolodental increment; BDH, decrease
in body height.
                                            FABLE 2
      COMPARISON 01 EXPIERIMFNTAL AND SHAM HEMIMANDL3ILLS IN I-HE ENUCLEATlION SFRIES
                                     Experimental           Sham
                                 Hlemimandible (mm)   Htemimandible (mm)          Mean
                                      (N   13)               (N   13)           Difference              Level of
      Variables                    Mean      SD*         Mean         SD          (mm)         t      Confidence
Mandibular length                 21.01      0.78       21.56        0.68         0.55        1.98      0.05
Ramus width                       10.40      1.09       10.67        (.88         0.27        0.70
Mandibular body height             5.07      0.33        6.77        0.20         1.70       16.661     0.1I
Medial shift of mandible           2.38      0.56        3.99        (.15         1.61       10.25      0.01
Alveolodental height               3.30      0.45        3.17        0.27         0.13        0.86
  * SD, standard deviation.

                                              'IA B LE 3
      COMPARISON     OF   EXPERIMENTAL AND SHAM H1-EMIMANDIF5LES IN THE CONDYLECTOMY SERIES
                                     Experimental           Sham
                                 l-lemimandible (mm) Hemnimandible   (mm)         Mean
                                      (N    13)             (N   1--3)          Difference             Level of
      Variables                    Mean       SD*       Mean             SD       (mm)         t      Confidence
Mandibular length                  16.43     0.46       17.01            0.49     0.58        3.23      0.01
Ramus width                        11.01     0.74       10.77            0.98     0.24        0.68       ...
Medial shift of mandible            3.80     0.51        3.98            0.49     0.18        0.88       ...
  *   SD, standard deviation.
360     CASTELLI, RAMIREZ, AND) BURDfl)lI                       J Dew Res   March-Aphl    197.7

  Fici 3. Condylectomny provoked significant decrease in mandibular length as seen in operated
on (OH) and control hemimandible (CH). Skull in A shows normal occlusion and vertical
dimension patterns.

sion'.; (2) the enucleation of the incisor      main vascular supply of the mandibular
germinal center, which left a large space in    body.
the mandibular body that filled with a            In another project in this laboratory, six
slowly organizing blood clot: and (3) the       hamster heads were injected with different
loss of the inferior mandibular artery, the     dyes for vascular studies. They showed that
Vol 50 No. 2                                                                                 MANDIBULAR GROWTH IN HAMSTERS                 361
                                                                                                 the arterial supply to the mandible was
                         O
                                                                                                 regional in distribution and, in this sense,
                                                      .
                                0
                                    .       *

                                                 0o                   0
                                                                      o
                                                                           .
                                                                                                 comparable to that of humans,'1 Rhesus
                         Q                                                                       monkeys,'2 rats,'3 and guinea pigs.'4 There
                                                                                                 was no evidence of an effective collateral
         u0
                                 t          N    O00                 IC)~ 00                     circulation that would take over the nutri-
                                                                     "I
                                                                               o
         4t                    ".*
                               el       t:            l                   r. cl                  tion of the bone where the enucleation was
                                                                                                 performed. Consequently, the nutrition of
         CC)
         H
                                                                                                 the region was temporarily mediated by the
                                                                                                 organizing blood clot through a process that
                                      r) 00 \O                       C0        11
                                                                                                 has been called serum imbibition.15 With
         V         0     OS
                               r- 0                                  '-0l~rW                     bone substrates, however, this type of nu-
         H                                                                                       trition has to be limited in scope.'6 Thus,
                                 *n         *~ *                     I*                          the interruption of inferior alveolar artery
         z                                                                                       supply provoked a localized ischemic re-
         0         401         C o
                                o- oNo
                                                                                                 sponse, that was accompanied by a slow
         ¢                                                            o
                                                                                                 repair process of revascularization, reossi-
         4:
                                                                                                 fication, and resorption of necrotic bone.'7
         0                                                                                       Each of these previous events have ac-
                                                                     00 00                       counted for the altered mandibular mor-
                         cfs                                                                     phology seen in the enucleation-extraction
        H;
         z-                                                                                      procedure.
         0                                                                                          Absence of teeth, along with the alveolar
         Q;                                                                                      bone atrophy, consistently reduced the body
               0'!-      r.                 .    %o                                              height in experimental hemimandibles. Com-
                                                                               Co
               0         c        .         .
                                                 'I                        *
                                                                                                 pensatory functional mechanisms that, for
                                                                                                 the most part, involved the masticatory
         EH
                                                                                                 muscles attempted to bring the affected
               I..,
         z     UC)3                                                                              mandibular side back into occlusion, caus-
         Q
                                  .         .   *It1m6                         ON
                                                                                                 ing the experimental sides to shift medially
                                                                           *
                                                                                                 and cranially. The medial pterygoid muscle
         4                                                                                       appeared to be the primary muscle involved.
                                                                                                 The decrease in body height, seemingly, was
                                                                                                 offset in some specimens by an abnormal
         z                     en C-C
                               C5.~
                                        i   .
                                                                                                 growth of the alveolar dental processes in
                                                                                                 the hemimaxillas. Computer analysis re-
         CC    C (C
               0
                                                                                                 vealed these elongations were not significant
                   I                                                                             (Table 2, Fig 2).
                               0000                                  00
                                                                      O
                                                                                                    As a consequence of the medial move-
                               o.~ cl
                               C)000
                                                                     r-
                                                                                    -            ment of the experimental sides, it was ex-
         Q                                                                                       pected that a lateral compression of the oral
         ¢                                                                                       viscera, such as the tongue, and nearby
         z                                                                                       structures and regions, such as the sublin-
         z                                                                                       gual gland and pharynx, would displace the
                                                                                                 sham hemimandibles laterally. A slight dis-
                                                                                                 placement was produced, as shown by a
                                                                                                 comparison of the gonion-bulla distance
                                                              C-)                       X        between sham hemimandibles in enucleated
                                                                                        CZ       series with contralateral sides in control
                                                              cd
                                     4.-'
                                                                                                 hamsters (Tables 2, 4).
                               Cd
                               '0                     Cd                                            The enucleation procedure was respon-
                                                              s...
                                                                                                 sible for a significant decrease in the length
                                                                                                 of the mandible as judged in terms of sam-
                                    ;-                                         C
                                                                                                 ple size and probability value. Hamsters
                                                          C    Z
                                                                                                 3 weeks old have molars already erupted
                                                                                                 and incisors that function. Different results
362     CASTELLI, RAMIREZ, AND BURDI                             I Dent Res March-April 1971
may   have been obtained if    younger   ham-    impaired nutritional circulation because of
sters were used.18                               enucleation procedures. In hamsters with
    A general analysis obtained in the con-      condylectomies, the length of the experi-
dylectomy series confirms previous findings      mental hemimandibles was reduced rou-
by Giannelli and Moorrees'8 and Sarnat and       tinely because of the loss of the articular
Engel,19 who found that condylectomies do        cartilage and subsequent impairment of
not modify occlusion as judged by normal         ramal growth. No changes in occlusion and
jaw relationships. The only variable that was    masticatory function were noticed in this
 altered in this series was the mandibular       series.
length, supra-angular notch-infradentale dis-
tance. The studies of Enlow,2 Enlow and                            References
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