Effects of Dietary Consistency on Craniofacial and Occlusal Development in the Rat

ROBERT

M.

BEECHER AND ROBERT

S.

CORRUCCINI

Dr. Beecher is Assistant Professor, Department of Anatomy at Wright State University in Dayton, Ohio. He is a graduate of the University of Virginia, and holds a Ph.D. degree in anthropology from Duke University. Dr. Corruccini is Assistant Professor, Department of Anthropology, Southern Illinois University in Carbondale. He is a graduate of the University of Colorado, and holds a Ph.D. degree in anthropology and paleontology from the University of California at Berkeley. Address: Dr. Robert M. Beecher Department of Anatomy Wright State University Medicine Dayton, OH 45435

Moderate differences in the hardness of diet are related to significant differences in maxillary width and other measures of facial size. Probably even more important is a relationship to the coordination of growth of different parts of the dentofacial complex. Muscular stimulation mediated through occlusal function seems to play a significant role in the coordinated development of facial structures.
MODERN DIET AND MALOCCLUSION

School of

This study was supported by a Biomedical Research Support Grant from Wright State University.

The prevalence of malocclusions in an urbanized society such as the United States is so high (50%1) that one is led to suspect the involvement of environmental factors in the etiology. Non-western, hunter-gatherer peoples are characterized by much lower frequencies of malocclusion." However, the transition of peoples from rural or aboriginal to urban or industrial living has been rapidly followed by an increase in the incidence of malocclusion. This increase is found whether comparing medieval Europeans to recent ones--- or nonwestern peoples to their immediate descendents living in a westernized environmen t. 2,5-15 There is a strong genetic factor in the development of occlusion. Occlusal patterns within families have been demonstrated to be heritable to some degree,16,17 and ethnic groups have been characterized by the frequencies of particular occlusal patterns.18-21 61

Vol. 51

No. I

January,

1981

62 Beecher and Corruccini probably due to a reduction in muscle use rather than increased. The rapid increase in the incidence of malocclusion (often within one generation) gives cause to look beyond genetic explanations such as relaxed selection pressures. growing animals responded to this stress by skeletal adaptations.> Disrupted occlusion The prevalence of an occlusion that varies from the ideal is not the norm among mammals. specifically: (1) some posterior bone deposition. mouth breathing is probably a factor in the development of human malocclusions. (3) lengthened condylar neck. Hiniker and RamsIjord= also found dentitional changes as teeth were forced to move to maintain occlusal relationships. (2) placing devices in the mouth to effect alterations in mastication. abnormally-directed muscle tension. While the younger. racial outcrossing. Several workers have applied stress to the masticatory apparatus or have altered occlusal relationships using appliances fastened to the teeth of rats or rhesus monkeys. (2) bone resorption of the anterior edges of the glenoid fossa. Experimen Is in effects of function Apart from radical surgery. These are usually designed to force protrusion of the mandible 1. Schultz= documents that dental crowding is quite rare in primates} and neither any of the specimens he presents nor any of the 400 wild primate dentitions that one of us (RSC) has examined would rate a Treatment Priority Index (TPI) score higher than 2.0 mm in order to achieve molar occlusion. Mouth breathing Mouth breathing has been implicated experimentally (using macaques) in the development of open bite and or an abnormally narrow maxillary dental arch. older animals responded with tooth movements to adjust to the new occlusal alignments. (3) restricting animals to calorie-deprivation diets.5-2. especially the physical consistency of the diet. This movement resulted in short-term periodontal traumas which abated when The Angle Orthodontist .vSuch effects are common in humans. and (4) varying the consistency of the diet from hard to soft. or accumulation of genetic mutations. we believe that environmental factors. and ('1) an increase in the angle formed by a line running from the condyle down the ramus with the line representing the occlusal plane. Using mature animals and a splint on the anterior teeth to force mandibular protrusion.sv-" A crown on the maxillary buccal teeth of rhesus monkeys was used by MeNamara-" to force the mandibular molars to occlude slightly lower than the normal occlusal surface of the uppers. inbreeding. Based on the available anthropological and experimental evidence. the experimental attempts to induce developmental change in the mammalian masticatory apparatus have used four methods': (I) forcing mouth breathing in animals. Similar differences were also found in soft-diet rats. The maxillae of these animals showed reduced vertical and prognathic growth. affect the developing masticatory apparatus and create variations in the occlusal phenotype. A cornman habit in childhood. Mandibular protrusion in young animals resulted in changes in the temporomandibular joint. attributed to altered muscle tension as the mandible is held slightly depressed during respiration.

Nutrition Experiments concerning the contribution of nutrition to normal occlusal development have taken the form of calorie deprivation of pigs. Tonge and McCance. All mandibular structures related to chewing were affected by diet hardness." and Henrikson. which resist bite (especially incisal) reaction force. and COX. were smaller. where toothfood-tooth contact takes place. and (2) "greater delay in the development and growth of the jaws.29 McCance. (4) had less width of the maxillary dental arch. The smaller masticatory muscles in soft-diet animals were almost certainly a result of lower work requirement in mastication. they do not create conditions likely to be encountered by the developing human masticatory system. Sagne and Thilander. were smaller.32 Moore. there is no evidence to correlate this deficiency with the occlusal problems found in so many urbanized peoples of the western world. (3) had mandibles that were smaller. Watt and Williams. While calorie deprivation is undoubtedly a factor to consider in severely undernourished people. Attachment areas for the jawclosing muscles." Barber. Vol. Rehabilitation was only partiall y successful. the animals were maintained for approximately four months. Beecher and Corruccini35 examined a small population of rhesus macaques which had spent a short period during adolescence on contrasting hard/soft diets. Green. Owens and Tonge= used weanling animals. They . Dietary consistency Although many workers have commented on the probable influence of the hardness or softness of the diet on the developing masticatory system. the soft-diet animals: (I) were slightly smaller in body mass. (5) had smaller masseter and temporalis muscles. where muscle force is transmitted to the mandible. The authors found that their regime resulted in: (I) delayed dental development and eruption. (2) exhibited no molar wear. In all studies. with condyles smaller and radiographically less dense. before attempting to "rehabilitate" some with proper foods."29 The consequences were tooth crowding and abnormal tooth-tooth contacts. the growing skeletal system adjusts. was less. Even buccolingual thickness of the mandible. which is essential to resist transverse bending. 51 No. Wear of the molar.Diet Consistency jOcclusal the teeth adapted and once again occluded adequately. When compared to the harddiet rats. and (6) had skulls consistently smaller in mass and in linear dimensions. although with no significant differences in shape. The condyles. 1 January. The smaller and less-active muscles applied less stress to the bones. More recently. especially in the mandible.used weanling rats divided into populations eating either pelle ted rat chow as a hard diet or crushed or water-softened chow as a soft diet. While these experiments are important in assessing the response of the masticatory system to unusual mechanical stress. the dentition migrates to accommodate. was less in the soft-diet animals. in older animals.28. maintaining them for one year on a severe calorie-deficient diet. These studies demonstrate that forced realignments of occlusal relationships and mandibular movements lead to responses by the most flexible elements of the masticatory apparatus. which responded with less deposition and growth. In young animals. 1981 Development 63 four studies have examined this idea experimentally.

finds the major axes of the between-variable correlation matrix. resulting in a lj uantum change in the morphology of the masticatory system. Ninety animals were divided into three groups: Group I was fed pelletted rat chow (Purina Formulab). related to factor analysis. the heads were randomly numbered so that the measurer would not be aware of their group membership. Fresh mass of the entire masseter. there has been no attempt to integrate these data in such a way that interactions between different parts of the growing masticatory systems could be measured. incisor to distal edge of last molar. This correlated with the histological findings by Bouvier and Hylander-" that significantly fewer secondary Haversian systems were present in the mandibular corpus of soft-diet monkeys than in the hard-diet monkeys of the same population. The eigenvect. Least-squares theory is used to rotate orthogonal axes to a position where the major axis subsumes a maximized amount of the total variance. with only two groups. acquired at 21 days of age. 2. A principal components analysis was performed on the data in order to discover t. It was to fill these gaps in the experimental record that the following study was carried out. The second axis is the axis perpendicular to the first that subsumes the largest possible amount of residual variance. with dry pellets provided every seventh day only. Group II I was fed the soft diet six days. evenly divided between males and females. and so on. Body mass. 'While a number of measurements have been taken from animals in dietary consistency experiments. Mandibular length. MATERIALS AND METHODS The experimental animals were Sprague-Dawley rats. 4. incisor to Ml. 5. it could not be determined whether the masticatory system responded in direct proportion to differences in dietary consistency. the same length of time used in previous experiments of this type. hard and soft diet.ors (also known as directional cosines or latent vectors) summarize the multiple interplay among variables. We have no way of knowing the consistency of rat diets used in earlier experiments of this type. Further. easily breaking down into small granules. Croup 11 was fed a gruel-like porridge consisting of ground chow moistened with water. Maxillary arch breadth across buccal points of ?vII. After sacrifice. Measurements Crable I) were taken as follows: 1. Animals were also examined for visible differences in tooth alignments and attritional differences between the three groups. 3. We found the lab chow to be crumbly. engendering only subtle differences in bite force. Anteroposterior length of condylar articular surface. 6. This indicates that the "hard" diet was minimally harder .he correlations among the several variables. or whether no differences should be expected until a threshold in dietary consistency difference was reached. Maxillary arch length. The three populations were maintained on their respective diets for four months. Projection of indiThe Angle Orthodontist found significant narrowing of the maxillary arch with no lessening in length in the soft-diet monkeys.64 Beecher and Corruccini than the gruel. This technique.

..26 38. Masseter weight (gm) . a result attributable to the small differences in dietary consistency.) 24. Dispersion.39) (11..31 39.57 4. the maxillary breadth is markedly increased in the hard-diet reared animals (Group I).00 9. Maxillary Breadth (mm) .40) ( 0.79 9.1 January.. Table 3 lists key paramo eters of this analysis. Condyle Length Body weight (gm) . the second axis is largest among the softdiet animals.03 1.43 ( 1. Breakdown in growth coordination Mcxillary breadth affected most The basic descriptive statistics in Table I show the hard-diet population (Group 1) to be larger in all dimensions and disproportionately so in some. For instance. but not significantly so.. Group III is intermediate in standard deviation. The population reared on an intermittently hard diet (Group III) is generally intermediate in the size of structures. • 3-sample TABLE I and Significance of Difference Hard Mean (s. Variable Maxillary Length (mm) .d.89 3..) ~:I.f. 1981 .58) ( 0.56 ( 1. The gross differences in the growth of most structures are not very marked.d. In particular. and the differences are often significant.36) (9. Again.39 8.64 8. significant < .38) ( 0.65) ( 0. which is much more integrated with growth in the condyle and upper arch breadth in hard-diet than in soft-diet animals. Mandibular Length (mm) (mm) . All correlations are higher in the animals that had more masticatory resistance.50) (0.17) ( 0. The strongest difference is in the growth relation of the masseter muscle.) 23.44 at p (0.45 8. Vol. signifying that all structures are more tightly integrated in their growth and covariation.20) ( 0.48) Soft Mean (s. The major (coordinated growth) axis is largest in the hard-diet sample. Thus the residual from Mean. Table 2 indicates the pairwise correlations in the hard and soft diet groups (I and II).43 43..38 2. but usually closer to Group I. although more similar to the soft group. RESULTS Development 65 more variable than Group I in the maxillary arch measurements.40) om AoV with 2 and 87 d.91 3.32) (0..72 1. Group I is more variable than Group II in every measurement. Inversely related to this. greater variation away [rom a major principal components axis describing general growth could be interpreted as meaning that there is poorer coordination of regional growth rates in those individuals.21' 1.~6) (0.d. 51 No..01) lAO ( 0.7 I 9.41) (12. The comparison of correlation structure can be more easily accomplished through examination of the principal components of the correlation matrix. this measurement alone shows a differentiation that is too large (relative to within-sample variation) to be reasonably ascribed to chance. indicating a greater range of sizes. Group III is slightly A much more obvious feature of difference is manifested in the COl'relation structure between measurements within samples.18 lAO Intermittent Mean (s.88) (0.05.28) (or Measured Traits F 0.Diet Consistency jOcclusal vidual cases onto the principal component axes allows interrpretation of multivariate variabilitv within samples.46) ( 0.92 3. and functional interpretation of the morphological integration among variables..

60 0.... In all respects.05.74 0...85 Groups Mussel... at the stage of growrh...38 Attrition not affected the major growth aXIS (which could be interpreted as error in growth or variation in growth rate) is easily largest in the soft diet sample.91· 0. Body weight . The Angle Orthodontist ..H3 0.71 Soft diet ~ r in hard < . the intermittent-harddiet group (III) is intermediate when compared with Groups I and 11 but more similar to the hard-diet sample.66 Body 0....Ve examined the occlusal surfaces of the rat molars as a further test of the comparability of our hard chow and that used thirty years ago by Watt and Williams. a decrease in correlation of masticatory structures is more noteworthy than de- = '."] ""hile they noted easily observable differences in attrition between soft and hard diet groups...19.75· 0.54 0. Masseter weight tends to be inversely correlated with maxillary breadth and condyle length on the second axis in soft animals. ~ e: 0.5%. Mandibular Length . IMaxillary Length . most chewing stress has been removed and little bite force is now called into play in the jaws of the growing child.. We noticed no displaced or rotated teeth in any of the animals...89 0.39 diet sample at p :c . Only in the 19th and 20th centuries (il apIJcars) has food become so processed tha t for practical purposes... 0. Masseter weight .... Ii Mand. DISCUSSION Present-day insults to occlusion Oppenheimer" and Lavell-v document the better occlusion that existed in human populations prior to the onset of the industrial revolution. • Significantly larger Max.. we could find none..72 Condo 0.37.78 0. This increased multivariate variability in soft-diet animals is all the more striking in view of the fact that they were less variable than the hardfood animals in every univariate trait. which is significantly greater than expected by random error at P 2.L 0. . TABLE 2 Product-moment Correlations Among Variables Within the Soft (lower triangular half of matrix) and Hard (upper triangular half) Dietary Max..79· 0.66 Beecher and Corruccini crease in size of the structures that seems to follow with a stronger dietary differentiation. condyle length. Thus.. No caries were observed by us in any animals.83· 0. The correlations of variables with the axes show that the breakdown in growth coordination in soft-diet animals is especially marked in maxillary breadth. Maxillary Breadth ..... Condyle Length ..55 0.93· 0. Perhaps a decrease in buffering among the growing components is the first step in their decrease in size.... This phenomenon has also been noted in characters that are diminishing in size through natural selection.... . Condyle length alone shows a notable residual on the second axis in Group I and III...79· 0. and masseter weight... the F-ratio of variation on axis two (dispersion from axis one) between soft and hard samples is 2..differentiation represented by this difference in dietary consistency.

1 January. Thus. considerable evidence ties upper-lower correlation diminution with development of mal- TABLE 3 Eigen Values (latent roots) and Eigenvectors (latent vectors) of the Correlation Matrices in Three Dietary Groups Principal Component (coordinated Hard Soft EigenValue ('70 variance) Eigenvector correlations: Maxillary Length Maxillary Breadth Mandibular Length Condyle Length Body weight Masseter weight 4.59 -0.42-45 The growth independence of mandible and maxilla in humans has been frequently noted. prenatal insult.97 0.50 (8) -0.90 0. as shown by the tendency of some indi- Development 67 viduals with anodontia to have average-size mandibles.29 0. disturbance of synchronous development in separately growing parts.51 0.06 -0. but does not give the source of the growth-correlation breakdown.89 0.80 One Principal Component Hard Two growth) Intermittent 4.w Moorrees and Reed.12 0.:" Maxillary growth may be under closer genetic programming. with the maxillary teeth being more conservative and controlled by a fewer number of genes.73 -0. it clearly is not favored by many orthodontists as an explanation of the rising rate of occlusal variation in humans.67 (78) 0. since cases of anodontia show restricted growth while cases with muscular paralysis may develop normally.10 Vol.23 0. The aging process also yields different results in upper and lower arches. premature deciduous tooth loss. 1981 . hormonal intervention.04 0.Diet Consistency/Occlusal A number of other environmental factors have been suggested as influences on developing occlusion. Tooth spacing and crowding.57 -0.08 0. In particular.89 0. and independence of tooth formation.17 (69) 0.w Carrr" lists breakdown of synchronous growth in lower and upper jaws as a possible cause of malocclusion.79 (13) -0.94 0. trauma. the mandible may depend on muscular function to grow to average size." also stress the importance of high correlation between tooth and arch size to the development of good occlusion.82 0. Though the chewing explanation is most predictive of observed occlusal differences in the rats.41 -0. the reduction of chewing resistance and related growth stimulation provided by "civilized" man's refined diet may be the strongest causal factor in developmental malocclusions.41•42 Some of these may be of minimal or no importance.60 (10) -0.77 0. especially of anterior teeth.08 -0.05 -0.14 0.96 (83) 0. follows different rates and peaks at different ages in the maxilla and mandible.16 -0. Potter et alY demonstrate that upper and lower dental arches are under very different sorts of genetic control.96 0. 51 No.92 0.18 -0.68 0.95 (variation in growth) Soft Intermittent 0.95 4. experimental evidence which might weight such factors is absent.80 0.91 0. including mouth breathing.93 0.e-v Lower correlation between upper and lower teeth in maloccluded individuals (as compared with normal) has been noted by Lavelle.06 -0.90 0. endocrine disturbance. oral habits. Because of its widespread occurrence in western society.68 0. posture.

present convincing genetic arguments against this explanation. J. P.: Dental condition of two tribes of Taiwan aborigines-Ami and Atayal. II.. Klatsky. Solomon Islands.: The occlusion of the Australian aborigine. A. Kelly. teeth. J. Orthod.: Further studies on the Xavantc Indians. Tiss. J. Am. H. 2. Bjork.: Malocclusion and civilization. B. Assoc. D. In this animal population the disassociation in size of occlusal features during their growth. Washington. 11. K. Orthod.-A. Orthod. 45: 172-207. 1961.: Dental observations among the Eskimos. M. Price. Replication of these experiments with a laboratory animal more closely related to man in terms of both biology and masticatory system is seen as a vital future need.: Anglo-Saxon and modern British teeth. 9. R.1977. Am. Am. 1977. H. Vital and Health Statistics. and muscle function.: An assessment of occlusion of youths 12·17 years. W. Mediolateral maxillary growth seems dependent upon the muscular stimulation provided by rough elements in the diet. Am. L. a Melanesian group on Mailaito. Waugh. 1947. Dent. Periodont . Dent. 80-93. Am. lium. W. L. S. M. 1948. Res. Cotton. Eur . Takano. Res.: Investigations concerning the dentitions of the Eskimos of Canada's Eastern Arctic. Williams. J. and continual incisor function in rodents maintains a base level of function regardless of diet that has no parallel in man. 17. Genet. 13..: The Downs analysis applied to three ethnic groups. Arch.. 14. 1951. Dent. Kargar. Res. USPHS. 36:385. Hunt. W. J. Assoc. 60:344354. Waugh.: Eskimo and Indian field studies in Alaska and Canada. and Frei. J. 14:34. B. Lombardi. the inheritance of different-sized parts that must occlude is attributed to the independent segregation of disharmonious genes from disparate ancestors.. 7. 1937. The prevailing explanation for such lowering of growth correspondence has been the effect of racial admixture between populations. CONCLUSION We believe our results suggest future directions for fruitful research based on the following observations. The ora! status of the Xavantes of Simoes Lopes. 56:117-126. J. Henrikson. J. Phys. M. Angle Orthod.: Mal· occlusion in the Kwaio.: Studies in the dietaries of contemporary primitive peoples. 162.: Tooth-Size and Occlusion in Twins. The unfused mandibular symphysis in the rat alters force distribution. D. Clinch. 15. L. Tand. A. and Harvey. Chung et al. Niswander. IG:355-356. 10. Calci].: Influence of the diet on the jaws and the face of the American Eskimo. W. J. 1966. 23:417-437. 1977. 8. Trans.C. previously noted in certain groups of maloccluded humans and attributed to racial admixture. and Thilander. L. L. 18. 1972. No. C. 1. 1968. Kraus. Supp. 4. 1Dent. 5b). V. I'. Anthrop. 5. Goose. Am. 47:811815. Lavelle. A. 24:1640· 1647. Dent. 22:466-467.. 3. VI!. 1959. Oral Bioi.. 12. Wise. E. A.: Malocclusion in the modern Alaskan Eskimo. Suensk . 40 (Suppl. Dent. Sagne. H. 16. C.: Hered· ity and the craniofacial complex. Ortluul. 21 :213-220. 19. and Bailit. Alii.v-se Thus. 1951.68 Beecher and Corruccini REFERENCES occlusion in humans. and Wong. Lu. Soc. J.: Maxillary dental arch width in Chinese living in Liverpool. ~ 1. 1972. E. Lundstrom. R. has apparently resulted from lower chewing stress required by a soft dietary consistency. Assoc. Wood.: The face in profile. 47:406-422. 1976.: Bone. A iii. B. 1948. Res.. The Angle Orthodontist . J.°o and Lombardi and Bailit. 1937. 1943.. 19:543-553. S. C. D. 17:231-233. Basel. J.1936. Ser. 6. The amount of maxillary arch narrowing and collapse can be predicted by the amount of time the animals were chewing on hard food. W. 36:283·294.

J. S. 1973. N. 43:412-421. 1965. J. 1978. Malocclusion. and Kau.. A. J. and Weinstein. 31. and Dantuma. 29. 1966. D. J. 1972. 5:419-421. Maxillary and mandibular tooth size in different racial groups and in different occlusal categories. 12:77-88. J. 11.. M. Zool. J.: Severe undernutrition in growing and adult animals.. 19: 14-34. [rosthet. Am.. Anthrop. ]. Oppenheimer. L. and teeth of pigs. Anthrop.. 28. Smith. Am. J. L. A. 1973.. G. G.. 40. and Chierici.: Craniofacial variation in a central Australian tribe.: Variability in wild and inbred mammalian populations.: Neuromuscular and skeletal adaptations to altered function in the orofacial region.: Primate experiments on oral sensation and dental malocclusions. 15. E. Br. R. D.: A twin study of dental dimensions. Bouvier.Diet Consistency jOcclusal 20. Smith. 64: 578-606. 1951. M..J.. and nailit.: Masticatory function and skull growth. S. 41. Beecher. Moorrees.. J. L. Moore.: Variation in dental occlusion and arches among Melanesians of Bougainville Island. 61:29-37. Anthrop. Watt. 146:1-34. M.: Genetics of common dental disorders. R. J. L. Lavelle. J. 19:361-372. and Reed.. Am. Res. B. 59:1-IR. 43. B. and Hylander. H. B. Angle Orthod. Dent. Tonge. 47: 195·208. 19: 197-206. Am. J. 21. P. Tonge.: Research and malocclusion. Orthod. 1961. C. 73:895-928. Am. 1. C. and HermannStutzmann. sex differences and population comparisons.. R. 50. 1968. R. H. F. 1. C.. D. 1'.: Cenctic and epidemiologic studies of oral characteristics in Hawaii's schoolchildren. W.. 36. Dent.: A radiographic cephalometric study of the central Australian Aborigine.. Methods. and the delay and malocclusions produced by calorie deficiencies. J. W. New Guinea. in press. Rhinology XVI:191-196. 34. C. Sci. J.: Anterior displacement of the mandible in adult rhesus monkeys. Phys. D. J. McCance. jaws. R. and Corruccini. K. M. 1973. R. ]. T. K. Am. 51. Orthod.. S.: Variation in the secular changes in the teeth and dental arch. Master's thesis.: Normal development of the jaws and teeth in pigs. W. R. Hiniker.: Variability in characters undergoing rapid evolution. 1970. C. Thoma. 42. 49. 1969.: The effects of the physical consistency of food on the growth and development of the mandible and maxilla of the rat. 16:503-512. Barber. C. Owens. and BaiIit. 22. 1965. Mourrees. Strnad. H. J. January. Clin. P. C.: Severe undernutrition in growing and adult animals. Alii. an analysis of Microtus molars. W. 33.: Research related to malocclusion. Br. 1975. Guthrie. W. Chung. Charlier. J. 24:171. W. Vargervik. J. and McCance. in press. Brown. 23: 471-495. F. C. Papua. Am.. Development 69 26. 23. Florida Acad. 1976. Morph. II. J. J. Angle Orthod. 1973. Phvs. Ackerman. G. R. 35. Schultz.. 25. Orthod.: Effects of mandibular hyperpropulsion on the prechondroblast ic zone of young rat condyle. R. and McCance.. Niswander. 48. 45. Evolution 19:214-233. and Cox. Hum.. Green. 115: 1-22. Nance. L. 1977. P. 37. L. A. R. J. H. Bader. Orthod. 46. J. J. J. 27. Burstonc. 1938.. 1971. 1966. Weijs. H. J. M. Christiansen. S. Isaacson... H. 1965. R. 51 No. H.. The mouth.. 32. Petrovic.: The cause and effect of mouthbreathing as related to malocclusion. Morph..: Biometrics of crowding and spacing of teeth in the mandible.. Anat. A.: Tool use and crowded teeth in Australopithecinae. and Shapiro. L. 47:6577. A. R. 22:257-268... 63:494-508. Orthod. J. L. The effects of rehabilitation on the teeth and jaws of pigs. R. 1.. J. A. McNamara. C. Orthod. Gam. Craven.: Effects of dietary consistency on maxillary arch breadth in macaques. Vol. Nutr. Nutr. A. age changes. Runck. 58:565-577. 28: 12·35. C. C. 44. 1975. Niswander.: Effects of bone strain on cortical bone structure in macaques. 1978.: Reply. Genet. 1963. 55:71-74. Curro Anthrop. Independent genetic determinants. Lavelle. J. K. 1971. Res. Hixon. 38. J. Orthod. Am. 47. Dent. J . Dent. n. II. Am.: A genetic study of class III malocclusion. C. 1981 . University of Adelaide... and Davis. 44:397412. 1954. E. Yu. V.. Harvold. A III. R. and Tonge. Litton. 146: 123-131. S. Curro Anthrop.: Problems and methods in research on the genetics of dental occlusion. Am.: Electromyography and mechanics of mastication in the albino rat. S. D. Orthod. 39.-P. Bilben.: Effects of the ph ysical consistency of the diet on the condylar growth of the rat mandible. Orth od. S. 18. 47:661-673. Potter. Phys. 1956. and Williams. 1.. 1965. Am. 24. ]. and Ramsfjord. 6:356357.' 1. 42:848-851. J. 30. Am. W. J. Angle Orthod. E. M. 1958.: Principal factors controlling development of the mandible and maxilla. 1966. S.