DENTAL CARIES I N PERUVIAN SKULLS’ T. D. STEWART Division of Physicd Anthropology, United States National Museum In the course of preparing an essay on the changes which have taken place in the concepts of the etiology of dental caries,2 the writer was greatly impressed by two features of the literature, namely, the frequent reference to a varying racial resistance to caries, and, secondly, the failure in most anthropological reports on caries to fully analyze the material for causal factors. It has been customary to ascribe to race those variations in the frequency of caries for which other causes could not be found. Such statements, together with the many anthropological reports showing the enormous racial variations in the incidence of caries, have led many workers, unfamiliar with present etiological concepts, to overestimate the r81e of race in this disease. This has even led some anthropologists to use caries as a criterion for race mixture, particularly in cases of mixture with whites. CAUSES O F CARIES Because of our present knowledge of the causes of caries, which seem well substantiated by observation and experiment, it should be stressed that the gross variations in racial incidence can be accounted for on the basis of some form of malnutrition. Just as in the ossification of the skeleton, the teeth, during their formative period, are affected by changes Read before the second meeting of the American Association of Physical Anthropologists, Cleveland, 1930. * Originally prepared for the pathology department of the Johns Hopkins Medical School, then summarized for the first meeting of the American Association of Physical Anthropologists, Charlottesville, 1930,with the title, ‘ ‘Anthropological interest in dental caries.” 315 AMERICAN JOURNAL O F PHYSICAL ANTHROPOLOQY, VOL. JAWUARY-MARCH, 1931 XV, NO. 2 316 T. D. STEWART in metabolism, whether due to improper diet o r disease. The resulting hypoplastic tooth is believed to be especially predisposed to decay. It is now believed, therefore, that all of the older classifications of predisposing causes, including such factors as developmental defects, malocclusion, etc., may be reduced to malnutrition, using the word in the broad sense here indicated. Besides this predisposing cause there have also’ been enumerated many exciting causes, such as bacteria, oral acids, attrition, food impaction, etc. Some workers have recently attempted to prove that a specific strain of bacteria is the chief exciting cause of caries, but the results are inconclusive. The same comment applies to the other factors. It seems safe, then, to assume that eventually the exciting cause will prove to be a combination of all those now enumerated, and that such a combination is effective only when the tooth is hypoplastic. I n no case has it yet been possible to prove the existence of a racial factor in addition to those above mentioned. Thus what has seemed to be evidence of racial intermixture has been shown t o be due to a change in diet. A fine example of this is t o be seen among the Alaskan Eskimos. Among those groups where the present generation has been raised on ‘white man’s food,’ both mixed and full bloods have very carious teeth. I n the older groups, on the other hand, not even maximal attrition has caused caries in more than 1 per cent of the population, owing to the rapid formation of secondary dentin. FACTORS TO BE CONSIDERED I N THE TABULATION O F CARIES The tendency of many observers to record the state of the denture without a very serious attempt to analyze the material f o r causal factors has probably resulted from the use of skeletal material, of which usually only small numbers, often fragmentary, are available. Of course, for such studies the living are much to be preferred, if only f o r the certainty of age and sex. However, a review of the data on dental DENTAL CARIES IN PERUVIAN SKULLS 317 caries as derived from skeletal material seems to indicate that more information than has heretofore been presented can be made available. Moreover, unless certain well-known factors, here enumerated, are taken into consideration, much of the data on caries will not be comparable. Relative susceptibility of tooth f o r m s By merely determining the percentage of individuals with caries, only a rough estimate of the degree of malnutrition is obtained. If, on the other hand, each tooth is considered separately, it seems possible to recognize whether or not malnutrition was present at various ages during the period of tooth calcification, which is about the first two decades of life. There is some evidence that the cachectic states of adult life make the teeth more vulnerable to caries, through the withdrawal of calcium, but this proces’s would seem to affect all teeth equally. Relative susceptibility of teeth of two jaws Probably of somewhat greater significance than the difference in susceptibility to caries of the individual tooth forms is that of the teeth of the two jaws. Most observers agree that the teeth of the maxilla are more frequently carious than those of the mandible. No explanation has been suggested for this variance, and it is possible that a racial influence map be detectable here, if at all. Relative susceptibility of tooth sut-faces Depending on the morphology of the teeth and also on the type of caries present, certain surfaces are more frequently attacked than others. Distinction should therefore be made between caries of the occlusional and of each of the four cervical surfaces. At present it is not apparent that any further significance can be attached to this variation. 3 18 T. D. STEWART S e x difference All observers agree that the two sexes differ in their susceptibility to caries, the teeth of females being more carious than those of males. This sex variation is supposed to be due to the effect of pregnancy on the teeth of the females, though Ziskin was unable to find any difference between the teeth of pregnant and iiulliparous women. Should this sex difference be unassociated with functional or nutritional factors, it is conceivable that true racial differences may likewise exist. It scarcely need be added that, f o r accuracy, skeletal material must be sexed only by experienced workers. A g e incidence The last factor to be mentioned, and yet the one most important in deciding the incidence of caries, is age. Caries increases directly with age, and hence two groups of different mean ages a re not comparable. Too often in anthropological reports, where caries is considered, age is either ignored or the criteria for its determination are not stated. The determination of age in skeletons, after the period of epiphyseal union, is most difficult, even for the experienced. Moreover, in the study of caries, the state of the denture should not be used as a measure of age, for there is too great a tendency to place the more carious teeth into the older age groups. The criteria used in the present study are suggested as a solution for this problem, though it may be necessary to broaden the young age period where less material is available. I n brief, then, an adequate racial study of dental caries should consider the relative susceptibility of the surfaces of the individual tooth forms of both jaws, controlled as to age and sex. MATERIAL A N D METHODS The present study was undertaken with a view to applying the above conclusion to a primitive people and to one not previously studied. Of all the groups represented in the skeletal collections of the United States National Museum, DENTAL CARIES IN PERUVIAN SKULLS 319 the pre-Columbian Peruvians seemed to offer the best prospects of success. I n the first place, the number was sufficiently great to give large age groups in both sexes ; secondly, the material was well preserved, with relatively little tooth wear; and thirdly, caries was not extreme (in the next largest group, the Eskimo, there is practically no caries). These advantages seemed to outweigh such disadvantages as the extensive postmortem loss of teeth and the separation of the lower jaws from the skulls. That the material was deficient in these two respects is due to the fact that the remains were disturbed by gold seekers previous to their collection by Doctor HrdliEka in 1910 (Smith. Misc. Coll., vol. 56, no. 16, 1911). The extensive postmortem loss of teeth in this group rendered it impossible to study directly the susceptibility of the individual teeth to caries. Indirectly it was still possible to obtain these data through the antemortem tooth loss, assuming that such loss was due to caries and not t o alveoloclasia (pyorrhea) o r trauma. As it was not customary among these people to knock out the incisors and as accidental trauma to the teeth is of relatively rare occurrence, there remains only alveoloclasia to be ruled out. The destructiveness of alveoloclasia may be estimated by observation and more exactly, a s Leigh has shown, by measurement of the cervical exposure. As a rule, however, alveoloclasia increases with age, so it seems certain that in the early age group to be described this disease could not have caused any of the antemortem loss. It may be added also that the distinction between antemortem and postmortem tooth loss was never in question, while, on the contrary, i t was impossible to distinguish between third molars lost antemortem and those congenitally absent. Although the collection consists of both skulls and lower jaws, it is impossible to mate them. This is a more serious disadvantage to the present study than the postmortem loss of teeth, because age and sex are more difficult determinations in the jaw than in the skull. The best that could be done, therefore, was to make two series of the jaws, one presumably 320 T. D. STEWART of males, that is, characterized by general massiveness and squareness of chin, etc. ; the other, of females, or those lacking the masculine features. Ages of the jaws could not be determined. No selection was permitted, except in the exclusion of the completely edentulous. A limit was placed at one hundred of each sex. It thus becomes evident that data on the lower jaws are not directly comparable with those on the skull. The secondary sex characters are well developed in Peruvian skulls and sexing is not difficult. All sex determinations had previously been made by Doctor HrdliEka and the error from this source is minimal. As already stated, it is desirable to have an early age group of each sex, the criteria for which do not include the state of the denture. Of such criteria, only two seem quite practical in the unsectioned skull, namely, closure of the basilar suture and beginning closure of the sagittal suture. Of all the sutures, the sagittal is the only one in which endocranial closure is readily observable in the unsectioned skull. By the time the teeth have finished erupting, the basilar suture has completely closed, and then a short period intervenes before the beginning closure of the sagittal suture, as observed either ecto- or endocranially. The time period thus delimited is brief, in the early twenties, and certainly before the destructiveness of alveoloclasia and attrition has begun, It is not believed that sufficiently sharply defined standards exist for more advanced age groups, hence in the present study all of these are grouped together, forming a series of one hundred of each sex. I n the racial group under consideration it is interesting to note that the group of one hundred young females was more easily procured than a similar number of young males, whereas, of the older groups, the reverse was true. This difference in the mortality rate of the two sexes is thought to be due to the presence of a nunnery at Pachacamac, from which vicinity most of the material was obtained. DENTAL CARIES I N PERUVIAN SKULLS 321 RESULTS I n general, it may be said that the teeth of the Peruvians a r e well formed and spaced; crowding of the teeth is relatively rare. Few anomalies a r e present and consist principally of supernumerary incisors and rotated premolars ; rotation of a canine was noted in one lower jaw. Attrition Three degrees of attrition were recorded: the first consisted of wearing down of the cusps, but with retention of the cusp pattern; in the second the cusp pattern was completely lost, but the dentin not fully exposed ; in the third there was complete exposure of the dentin. Exposure of the pulp cavity, which usually constitutes the fourth degree, was so rarely seen that it is not included. F o r such a classification to be of value the same tooth must be examined in each skull, because wear is unequal, being greatest in the first molars and least in the anterior teeth. The extreme loss of teeth made exact observation impossible, but the following general statements may be made: The young males divided about equally between first and second degrees of attrition, with very few showing either third-degree or no attrition. About half of the young females, on the other hand, showed firstdegree attrition, while the remainder were divided between second-degree and no attrition, with very few showing wear of the third degree. I n the older age group there was a much larger number with complete ante- and postmortem loss of teeth, but it was clear that most of the remainder showed third-degree attrition, with second and first degrees coming next in order. No difference between the two sexes was apparent in the older group. Antemortem loss I n table 1 is summarized the relative susceptibility of the eight tooth forms both in the upper and the lower jaw. As each series was too small t o show significant differences between the two sides of the jaw, both sides a r e considered 322 T. D. STEWART together. The table is self-explanatory, but the following points may be pointed out as especially important: Sex. The sex difference is quite apparent. Thus in the young group, of the 218 maxillary teeth lost antemortem, 44 per cent were in the males and 56 per cent in the females. I n the older group, and likewise in the case of the mandibular teeth, this sex difference is less pronounced-47 per cent in TABLE 1 Antemortem loss of teeth i n pre-Columhian Perucian skulls. Relative susceptibility of tooth forms ( b o t h sides) __ _ I 5.2 17.7 11.5 16.4 21.9 33.3 26.2 23.8 I (333 = 99.9%) 100 old females (377 = 100%) 100 adult males 100 adult females I 6.3 1 1 I 5.6 5.7 42 4.8 2.6 i 7.2 7.5 23.7 21.6 8.2 11.1 20.5 226 i 26.6 22.1 44 _ j 1 56 ~ - 23.7 47 24.6 53 38.2 47 33.3 53 the males, 53 per cent in the females. If pregnancy is to be considered the cause of this difference between the two sexes, these figures indicate that it is more active in the young group than in the more aged, which seems unlikely. Again, the size of the series may be responsible for these results. Sex cannot be shown to be a factor in the susceptibility of individual tooth forms. A g e . A comparison of the young and old groups shows that caries increases in frequency after the early twenties, as DENTAL CARIES I N PERUVIAN S K U L L S 323 would be expected. The degree of difference between the two groups is unimportant, because the mean age of the older group is not known. The important point concerning the older group is the fact that, with the greater tooth destruction, the relative susceptibility of the tooth forms does not appreciably change; the most that can be said is that the destruction of first molars equals that of the second and third molars only in later life. Lower jaws. The mean age of the lower jaws is probably below that of the older group of maxillae, but certainly not as low as that of the younger group of maxillae; hence a greater immunity of the mandibular teeth seems evident. There appears to be little difference in the relative susceptibility of the teeth of the two jaws, with the possible exception of the first premolar and the third molar. And here it must be kept in mind that congenitally missing third molars a r e included with those lost antemortem. Caries in teeth present In table 2 is summarized the susceptibility to caries of the tooth surfaces. As no caries w a s observed in the very few incisors present, the table shows only the number of caries found in each of the remaining six tooth forms. The small number of teeth present made it necessary to combine the two sides. Two types of caries were observed, one occurring on the occlusional surface of the crown, the other below the enamel line on the cervix. Crown caries appeared t o be due for the most part to maldevelopment, defects occurring especially along the grooves in the molars. Cervical caries almost always began on the approximal surfaces, undermining the enamel and ultimately encircling the neck. F r o m table 2 it will be seen that certain surfaces a r e seemingly more frequently attacked by cervical caries than others; f o r instance, the proximal surface of the first molar and the distal surface of the second. This type of caries has been described by both Chappel and Leigh, but without explanation f o r its cause or 324 T. D. STEWART TABLE 2 Location of caries in teeth of pre-Columbkn Peruvians ( b o t h sides) i ITOOTX Canine Old 8 Old? Young8 Young? Old8 Old Young 8 - Fast premola 1 (IBOUP - UPPER J A W Cervjcal Number - canes teeth 1 ~ Proxi. mal - 23 23 79 41 1 1 ! 2 2 - _ Crown caries LOWES JAW 1 Cervical j Number canes teeth Proxi. I DisCrown 1 I ma1 I tal I i Distal 1 II- -- _ 2 2 _ I - 1 46 t 43 Second premola ____ 1 First molar Second molar -___ Third molar Young8 I 148 Young? 111 Old S 93 Old ? 73 --_ Young8 62 Young? 35 Old S 35 Old Q 22 - I -- ' 2 5 3 - I __ -I 51 I 1 6 3 ~ 1 55 ~1 2 1 1 i 1 2 8 i 1 0 , 9 1 l 105 16 18 - :I' 2 I - affinity f o r certain surfaces. I t would seem that food impaction must play a r81e. DISCUSSION Our knowledge of the diet of the aboriginal Peruvians is limited to a number of vegetables, such as they were accustomed to reproduce as decorations on their pottery and remains of which have also been found in their graves. It is assumed also that the inhabitants of Pachacamac, being near the sea, were fish eaters. Such evidence, though very limited, points to a balanced diet. As regards disease, it is i o t known DENTAL CARIES I N PERUVIAN SICULLS 325 whether these people were infested with intestinal parasites or malaria. Evidence from the teeth would indicate that none of these factors interfered seriously with their physical development, for only a moderate degree of dental hypoplasia seems to be present. In contrast to the teeth of whites in which the first molar is almost uniformly destroyed before the third decade, the same tooth in the Peruvians was not destroyed as frequently as the other molars until perhaps the fourth decade. Since the first molar is calcified during the first six years of life,it seems quite certain that the nutrition during that critical period was fairly adequate. More comparative data must be available before further interpretations along this line can be made. Finally, if a sex difference in the susceptibility to caries does exist independent of the effect of pregnancy, and likewise, if a difference in the susceptibility of the teeth of the two jaws is not dependent on the morphological differences between those teeth, then it seems possible for a racial variation also to exist. Data on other races, satisfying the requirements here proposed, may lead t o the identification of such a racial factor. There is appended a short bibliography of some of the more important contributions, from the anthropological viewpoint, on the subject of dental caries. BIBLIOGRAPHY BOUVET,PIERRE1922 Lea lesions dentaires des hommes prehistoriques. Paris Thesis, no. 81. CAMPBELL, T. D. 1925 Dentition and palate of the Australian aboriginal. Publ. Keith Sheridan Found., Univ. Adelaide, no. 1. CHAPPEL, H. G. 1927 Jaws and teeth of ancient Hawaiians. Mem. Bishop Mus., Honolulu, 251-268. DAVENPORT, C. B., AND LOVE, A. G. 1921 The medical department of the U. S. Army in the World War, Washington, XV, I. GOBLIRSCH, A. W. 1930 A study of third molar teeth. J. Am. Dent. Assoc., XVII, 10, 1849-1854. HERPIN,A. 1911 Localisation de la carie sur les diverses dents. Bull. et MBm. SOC. d’Anthrop, Paris, 11, 578-586. KNOWLES, W. A. 1882-1886 Statistics of dental caries. Tr. Calif. Dent. ASROC., San Francisco, 112-120. 326 LEIGH,R. W. T. D. STEWART 1923 Incidence of caries in the different teeth and their respective surfaces. Mil. Dent. J., VI, 4, 183-194. 1925 Dental pathology of the Eskimo. Dental Cosmos, L X V I I , 884-898. 1925 Dental pathology of Indian tribes. Am. J. Phys. Anthrop., V I I I , 179-199. 1928 Dental pathology of aboriginal California. Univ. Cal. Publ. i n Am. Arch. and Ethnol., Berkeley, X X I I J , 10, 399440. 1929 Dental morphology and pathology of prehistoric Guam. Mem. Bishop Mus., Honolulu, X I . L E N H O S S ~M. K ,V. 1919 Die Zahnkaries einst und jetzt. Arcliiv. f. Anthrop., N.F., X V I I , 44-66. MAGITOT,E. 1878 Treatise on dental caries. (Translation.) Boston. MELLANBY,M. 1928 The influence of diet on the structure of teeth. Physiol. Rev., V I I I , 4, 545-577. MITCHELL,HELENS. 1930 Nutritional survey in Labrador and northern Newfoundland. J. Am. Dietet. Assoc., VI, 29. RUFFER, SIR ARMAND 1920 Stndy of ancient Egyptian teeth. Am. J. Phys. Anthrop., 111, 335-382. THOMAS,L. 1892 L’importance r6elle d e la distribution gbographique d e la carie dentaire en ethnographie. Odont., Paris, XJI. ZISKIN, D. E. 1926 The incidence of caries in pregnant women. Am. J. Obst. and Gyn., X I I , 710-719.