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 Harris,20 and Scott2l in humans have shown 1. SICHER, H.: Oral Histology, 4th ed, St. that the articular cartilage operates as a Louis, Mo: C. V. Mosby Co., 1965. growth site and is responsible for the up- 2. ENLOW, D.E.: The Human Face, New ward and backward elongation of the ramus. York: Hoeber Medical Division, Harper Based on the assumption that the articular and Row Co., 1968, p 134. cartilage in the hamster mandible performs 3. HARRIS, P.F., and WARD, P.H.: Unilateral a function similar to that of humans, the Hyperplasia of the Mandibular Condyle, decrease in length of the experimental hemi- Laryngoscope 78:1475-1486, 1968. mandibles would be related directly to the 4. Joo, Y.J., and KINNMAN, J.: Ankylosis of ramus rather than to the mandibular body. the Temporomandibular Joint, Laryngo- The present statistical study has helped scope 77:2008-2021, 1967. 5. BROMBERG, B.E.; SONG, I.C.; and RADLAUER, in the evaluation of the effect of the con- C.B.: Surgical Treatment of Massive Bony dylectomy and enucleation-extractions. Cri- Ankylosis of the Temporomandibular Joint, teria used were changes in mandibular Plast Reconst Surg 43:66-70, 1969. morphology, loss of normal occlusion, and 6. ANDERSON, D.E., and MCCLENDON, J.L.: spatial shifting of the experimental sides. Cherubism-Hereditary Fibrous Dysplasia of It was found that the enucleation-extraction the Jaws: I. Genetic Considerations, Oral surgery produced the most pronounced Surg 15(suppl):5-16, 1926. morphologic and functional alteration of 7. SCHLUMEBERGER, H.G.: Fibrous Dysplasia the mandible. The three principal factors (Ossifying Fibroma) of the Maxilla and Mandible, Amer J Orth Oral Surg 32:579- involved and responsible for these changes 587, 1946. were the loss of teeth, alveolar atrophy, and 8. WALDRON, C.A.: Giant Cell Tumors of the impairment of circulation to the mandibular Jaw Bones, Oral Surg 6:1055-1064, 1953. body because of vascular interruptions 9. WINTER, C.R., and MAIocco, P.D.: Osteo- linked to the enucleation procedure. De- genesis Imperfecta and Odontogenesis Im- tailed changes in vascular patterns of the perfecta, Oral Surg 2:782-798, 1949. mandible still need to be described in detail. 10. PIETROKOVSI, J., and MASSLER, M.: Alve- Condylectomies, however, did not produce olar Ridge Resorption Following Tooth any significant changes in the morphology Extraction, J Proth Dent 17:21-27, 1967. of the mandibular body that could lead to 11. CASTELLI, W.A.: Vascular Architecture of abnormal occlusion and/ or masticatory the Human Adult Mandible, J Dent Res 42:786-792, 1963. function. 12. CASTELLI, W.A., and HUELKE, D.F.: The Conclusions Arterial System of the Head and Neck of the Rhesus Monkey with Emphasis on the Enucleation of the incisor germinal cen- External Carotid System, Amer J Anat ter followed by the extraction of molars 116:149-170, 1965. in Syrian hamsters was directly associated 13. HUELKE, D.F., and CASTELLI, W.A.: The with several pronounced changes in man- Blood Supply of the Rat Mandible, Anat dibular morphology. These changes in- Rec 143:335-343, 1966. cluded a decrease in size of the mandibular 14. BOYD, T.G.; CASTELLI, W.A.; and HUELKE, D.F.: Arterial Supply of the Guinea Pig body, loss of normal occlusion, and a shift- Mandible, J Dent Res 46:1064-1067, 1967. ing of the mandibular body medially and 15. CONVERSE, J.M.; UHLSCHMID, G.K.; and cranially. These changes may be related to BALLANTYNE, D.L.: Plasmatic Circulation loss of teeth, alveolar bone atrophy, and in Skin Graft-The Phase of Serum Im-
Vol 50 No. 2 MANDIBULAR GROWTH IN HAMSTERS 363 bibition, Plast Reconst Surg 43:495-499, 19. SARNAT, B.G., and ENGEL, M.B.: A Serial 1969. Study of Mandibular Growth After the 16. COLLINS, D.H.: The Histological Structure Removal of the Condyle in the Macaca of Bone, J Bone Joint Surg 39B:770-780, Rhesus Monkey, Plast Reconst Surg 7: 1957. 364-380, 1951. 17. EDEIKEN, J.; HODES, P.J.; LIBSHITZ, H.I.; 20. ENLOW, D.H., and HARRIS, D.B.: A Study and WELLER, M.H.: Bone Ischemia, Rad of the Postnatal Growth of the Human Clin N Amer 5:515-529, 1967. Mandible, Amer J Orth 50:25-50, 1964. 18. GIANELLI, A.A., and MOORREES, C.F.A.: 21. Scorr, J.H.: The Growth of the Human Condylectomy in the Rat, Arch Oral Biol Face, Proc Roy Soc Med London 47:91- 10:101-106, 1965. 100, 1954.
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