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Dental Caries in Japanese Human Skeletal Remains
J. Oral Biosci. 51 （2）：105−114, 2009
REVIEW
Dental Caries in Japanese Human Skeletal Remains Hisashi Fujita§ Department of Anthropology, Niigata College of Nursing, 240 Shinnan−cho, Joetsu 943−0147, Niigata, Japan 〔Received on October 14, 2008；Accepted on March 8, 2009〕 Key words：dental caries／human skeletal remains／Japanese／anthropology／palaeopathology Abstract：The focus of the present study was dental carious sites in ancient Japanese skeletal remains, which has long been a focus of research. This topic is of interest because it has not received much attention. In addition, the causes of numerous incidents of root caries observed in the investigation of dental caries in ancient skeletal remains need to be examined. The results of this study indicated that there are more root caries than coronal caries in modern−day people. In Japanese people of the Edo period or earlier, the great majority of dental carious sites were on root surfaces. The cause was the loss of alveolar bone due to periodontal disease, and the cementum of the root was exposed, resulting in caries invasion of the exposed area. This sequence of events led to a pattern of dental caries and root caries in ancient Japanese people. This type of caries can be said to be of the elderly−type caries of the modern era. It is generally speculated that the advancement of physiological aging in ancient people was very rapid as they were under considerable physical stress. Unlike modern−day people, ancient people were unable to receive scientific dental treatment, and dental caries and periodontal disease were more frequent than expected. Using information gathered from investigations over many years, the historical changes in dental caries and the characteristics of dental caries in Japanese people from the Jomon period to the modern era are outlined.
Introduction Dental caries is one of the most common human “diseases”, along with the common cold. Signs of dental caries have been seen even in the early hominids, Australopithecine1）. Dental caries can be said to be a disease that has shared its path with human evolution. In anthropology, which deals with ancient human skeletal remains, the subjects of research include dental caries as well as enamel hypoplasia, dental attrition, and periodontal diseases. These diseases are a type of stress marker and are thought to be useful to §
Corresponding author E−mail：hfujita@niigata−cn.ac.jp
understand the oral hygiene conditions of ancient peoples and to reconstruct their biological and sociological backgrounds, which could be speculated from such conditions. In particular, numerous research papers on dental caries in anthropology deal with ancient human skeletal remains, and dental caries is the disease which draws the most interest. Dental caries comprises the most case reports in dental paleopathology because the teeth are the hardest tissue in the human body；therefore, even if ancient human skeletal remains are excavated in poorly preserved conditions, dental caries can be distinguished relatively easily and data can be accumulated for statistical analysis. Furthermore, an examination of dental caries enables speculation on various epidemiological factors of the time when these ancient people lived,
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including their oral hygiene, diet, and livelihood. As is commonly known, humans have undergone an evolutionary process from early hominids, Homo erectus, Neanderthal man or Homo heidelbergensis, to moderns humans（Cro−Magnon man and onward）. Unfortunately, fossilized human bones earlier than those of Homo heidelbergensis have not been found in Japan. Even modern human bones from the Pleistocene epoch are rare；therefore, human skeletal remains, including dental caries, that can be analyzed and statistically examined as a collection or“group” are from the Jomon period and onward2）. There are two methods of researching the diseases of our ancestors, and they are not restricted to dental caries research. One method is the study of medical history. This study is mainly on pathologies in ancient documents and literature and identification of the diseases. The second method is paleopathology, a field of study in physical anthropology. In this field, the study materials are archeologically excavated hard tissues, such as bones and teeth of people from ancient times. Of course the soft tissues have long ago decayed and returned to the soil；therefore, paleopathology allows the examination of the true pathological states of certain diseases at the time of death and the prevalence of the disease among certain groups of people. Sakura and Inoue et al. reported in their research changes in the dental caries rate using ancient human skeletal remains from Japan3,4）. Their studies were outstanding for that time, but the focus was on dental caries rates；therefore, the human aspects of the ancient people of the time could not be ascertained very well. As in medical history, the basis of paleopathology is the elucidation of disease and pathological states in ancient skeletal remains. In addition, it delves deeper to investigate the structure of disease at that time and to speculate on their society based on the structure of disease. Furthermore, paleopathology has great significance in probing various sociological and biological factors, including the diet, life span, childbirth, nutrition, and hygiene of the people. This paper investigated sociological and biological factors of different periods in Japan by following the changes in dental caries. It is based on studies focus-
ing on carious sites. Descriptions 1 ．High rate of dental caries in the Jomon people Study of the teeth of the Jomon people showed a surprisingly high prevalence of dental caries, although lower than that of the general modern population. When the dental caries rates of the Jomon people were compared to those from other societies of hunters and gatherers, people from other societies generally had lower dental caries rates2）. Table 1 shows the dental caries rates of people in similar stages of hunter and gatherer societies as the Jomon people and the historical changes of dental caries rates in Japan2,5―9）. The dental caries rates were much higher in the Jomon people than even the present day Inuits of Greenland or aborigines of Australia2,9）, and unlike any other hunter and gatherer societies in the world. Most hunters and gatherers who do not farm have very low dental caries rates. When their economy transitions from hunting and gathering to farming, the incidence of dental caries is known to increase sharply. In Japan, the dental caries rates increased sharply in the Yayoi people who adopted farming2,5,6）. The high dental caries rates in the Jomon people were thought to demonstrate the intake of large amounts of high starch foods which facilitated dental caries occurrence. In addition, they probably used food preparation methods that facilitated dental caries occurrence. 2 ．Importance of plant−based food Previously, people tended to think that hunters and gatherers consumed animal−based foods more frequently than plant−based foods but the proportion of plant−based foods that hunters and gatherers consumed relative to their overall diet was larger than imagined. This result is based on recent archeological findings and ethnological surveys from various foreign countries, and it is widely accepted today. Suzuki studied the food remains of the Jomon period and reported that nuts and wild tubers were very important as plant−based sources from the view-
107 Table 1 Dental caries rate of different economies and populations in the world Groups
Age
Economic level
Caries rate（％）& Source
Jomon（Japan） Yayoi（Doigahama, Japan） Yayoi（Mitsu, Japan） Kofun（Japan） Muromachi（Japan） Edo（Japan） Old Copper（USA） SJO−68（USA） Australian Aborigine（Australia） Inuits（Denmark） Inuits（USA）
12,000―2,300 yrs BP 2,000 yrs BP 2,000 yrs BP ca. AD 1700―1400 yrs ca. AD 1400 yrs AD 1603―1868 yrs 7,600 yrs BP 3,000 yrs BP Modern Modern Modern
hunting−gathering agriculture agriculture agriculture agriculture agriculture hunting−gathering hunting−gathering hunting−gathering hunting−gathering hunting−gathering & trade
8.22） 19.75） 16.26） 8.37） 14.63） 12.18） 0.49） 2.49） 4.69） 2.29） 1.99）
Caries rate（％） ：100（carious teeth／teeth present）
point of both calories and degree of edibility10）. He also indicated that the harvest times of fruits, leaves, and stalks were staggered, showing good distribution by season. Nishida studied the Torihama shell mound and reported that the largest proportion of total calories （43％）came from nuts, such as walnuts and acorns, followed by fish and meat11）. The most abundant food remains are of shellfish, which has relatively low calories. Thus, it was speculated that the main diet of the shell mound people along the coast consisted of plant−based foods. Minagawa conducted a very interesting study that investigated the diet of Jomon people by stable isotope analysis. He stated that the Jomon people probably consumed large amounts of plant−based foods. He believed that the Ainus in Hokkaido at that time consumed large amounts of animal−based food, unlike the Jomon people on Honshu12）. In actuality, the modern−day Ainus surveyed during the Edo, Meiji, and Taisho periods had a great preference for animal− based foods13）. It was reported that they even consumed the internal organs of the animals. This is very suggestive when considering that dental caries ；therefore, one prevalence is very low in the Ainus13） reason for the high dental caries rates in the Jomon people can be found in their diet, which was mainly plant−based foods.
3 ．Elderly−type dental caries in modern day Dental caries in the Jomon people can be compared with that in modern−day people. The present study focused on the sites of dental caries occurrence. The most common sites of dental caries are occlusal and interproximal areas in modern−day people, whereas the Jomon people were more likely to have dental caries in the interproximal areas, buccal cervical areas, and root areas （Fig. 1）, occlusal dental caries was 14） rare . The pattern of carious sites in the Jomon people is very similar to that in the modern−day elderly. The direct cause is exposure of the cervical and root areas due to the recession of gingiva and alveolar bone. Crowns are covered by enamel but cervical and root areas are composed of cementum；therefore, these areas are structurally weaker against the invasion of dental caries. Figure 2 is the oral image of a man in his 70s who presented at the Department of Dental Oral Surgery of the Tokyo Metropolitan Geriatric Hospital. His gingiva was inflamed, and his alveolar bone was receded. Unlike the Jomon people, this patient did not have buccal dental caries, probably due to the effect of brushing；however, the occurrence of root dental caries due to alveolar bone loss was determined to be almost the same as in the Jomon people； therefore, the pattern of dental caries in the Jomon people was similar to elderly−type dental caries in the modern day.
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Fig. 1 Root caries in the Japanese Jomon people（IDNO：131638 from Tsugumo site, and is housed in the University Museum, the University of Tokyo, Japan） .
Fig. 2 Root caries in the modern elderly people in Japan （This photograph is housed in the Department of Oral Surgery, Tokyo Metoropolitan Geriatric Hospital, Japan）.
Interestingly, researchers from various countries obtained similar results regarding cariaus sites in ancient man. Moore, Corbett, and Whittaker et al. studied dental caries in the ancient English15―17） and Lunt studied dental caries from prehistoric times and the Middle Ages in Scottish populations18）. All of these researchers indicated a high incidence of cervical and root dental caries. Two main factors explaining the above results can
Fig. 3 Occlusal dental caries in the Japanese Jomon people （young individual, IDNO：Satohama 15 from Satohama site, and is housed in the National Science Museum, Tokyo, Japan）.
be suggested. First, the progress of attrition was incomparably fast in people in ancient times and the Middle Ages relative to modern−day people. If dental caries in the occlusal pits and fissures was mild, the progression of attrition could have been faster than that of such dental caries；therefore, it is presumed that dental caries itself could have disappeared in many cases. This phenomenon is seen in modern Nigeria. Kubota et al. conducted follow−up surveys of people in Nigeria with dental diseases19）. Figure 3 shows occlusal dental caries in the Jomon people. Although the prevalence of occlusal dental caries was low in the Jomon period, it certainly did exist. Cusps and fissures were well preserved on this individual’s occlusal surfaces. An anthropologist familiar with the bones and teeth of ancient skeletal remains can easily determine that the individual was rather young；that is, such an individual with well− preserved cusps and fissures could have occlusal dental caries. The Jomon people were eating food much harder than that of modern−day people；therefore, their attrition was considerable. Occlusal dental caries was presumed not to have occurred in an individual with occlusal surfaces, such as those shown in Fig. 4. In other words, occlusal dental caries could be found in young people, but it became less likely in individuals beyond a certain age as attrition progressed with aging. If attrition was very considerable, mild occlusal
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Fig. 4 Severe dental attrition in the Japanese Jomon people （IDNO：130196 from Hobi site, and is housed in the University Museum, the University of Tokyo, Japan） .
Fig. 5 Pulp exposure caused of severe attrition in the Japanese Jomon people （IDNO：Hikozaki 6 from Hikozaki site, and housed in the National Science Museum, Tokyo, Japan）.
dental caries could have disappeared due to attrition, as in the aforementioned Nigerian cases. The causes of marked attrition of the Jomon people are probably also found in factors other than diet. As shown in Fig. 5, attrition of the anterior teeth could have occurred due to the use of teeth for hide tanning, just as in Inuits. It was speculated that teeth were used as“tools”. In this individual, the pulp cavities were exposed, and they were in a state of pulp exposure. Even if the Jomon people ate hard food, factors other than diet must be considered to explain the extreme attrition. The second reason for the high incidence of root dental caries is periodontal disease, which was speculated to have occurred at a very high frequency. Many excavated Jomon individuals had advanced alveolar bone resorption. As in modern−day people, bone resorption due to periodontal disease was seen in the Jomon people. The incidence of periodontal disease is closely associated with aging；therefore, a brief statement is provided below regarding aging and life span of the Jomon people. The average life span of the Jomon people has been provisionally calculated at approximately under 15 years for both males and females20）. This short life span was due to the remarkably high infant mortality rate, which reduced the overall life span of people in
the Jomon period. In anthropology, when studying a group with an extremely short life span, focus is placed on the average life expectancy of the 15−year− old survivors. This is an age at which a person gains some degree of resistance to disease. In the Jomon individuals who survived the first 15 years of life, the life expectancy was considered to be approximately an additional 15 years；that is, the average life span of such individuals was approximately 30 years. Even if some individuals had a life span longer than 30 years, the resorption of alveolar bone in the Jomon people was speculated to be 20―30 years faster than in modern−day people. This suggests that the Jomon people aged considerably faster than modern−day people and that periodontal disease was very common in a period without special measures for disease prevention and treatment. 4 ．Root dental caries is“ancient−type dental caries” As mentioned previously, dental caries in the Jomon people were found on the root surfaces in many cases, associated with loss of alveolar bone with periodontal disease and aging, and root dental caries in the modern’s elderly is similar to dental caries in the Jomon people. As shown in Fig. 1, root dental caries tended to be more prevalent than coronal
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Fig. 6 Occlusal dental caries in the Japanese Edo people（IDNO：Suzugamori M2 from Suzugamori site, and housed in the National Science Museum, Tokyo, Japan） .
dental caries in all time periods in Japan when human bones were examined from these periods.（There was no significant difference between the Jomon and Kamakura periods. When more materials are collected, a statistically significant difference could be indicated between these periods）. The incidence of coronal dental caries is significantly large only in modern−day people；therefore, root dental caries can be considered as“ancient−type dental caries.”Haraga et al. examined caries in Yayoi human skeletal remains excavated in northern Kyushu and found a high percentage of root caries in these remains. Their result is important as it is consistent with our findings21）. If there are many elderly individuals among the examined human bones, then the proportion of root dental caries is predicted to increase. If there are many young individuals, the proportion of coronal dental caries is predicted to increase. Human skeletal remains of the Kamakura period were excavated from the Zaimokuza site in Kamakura city, Kanagawa prefecture. Many of these individuals are considered to be people who died in action during the Kamakura attack of Y. Nitta during the fall of the Kamakura shogunate；therefore, they are thought to be relatively young. If there are many young individuals, the numbers of occlusal dental caries and coronal dental caries should be high. In paleopathology, using limited
materials, it is usually difficult to match the age of people in the group and to compare them under the same conditions. Root dental caries was prevalent in the ancient people of Japan because periodontal disease was prevalent and the root was exposed when there was no scientific dental care. In addition, the progress of physiological aging was markedly faster in ancient people than in modern−day people. It has been speculated that even at a young chronological age, people had periodontal disease. Figure 6 shows the dental caries found in mandibles of people from the Edo period. Occlusal dental caries advanced directly to the root area without affecting the surroundings in the coronal portion. This type of dental caries is seen in relatively young people in the modern day. In addition, this pattern of dental caries is almost never seen in Jomon individual, who had severe attrition. As mentioned in the previous journal issue, it was probably difficult for dental caries to occur on the flat occlusal surfaces of Jomon people who had considerable attrition, and mild dental caries probably disappeared due to attrition. Figure 7 shows the images of individuals estimated to be approximately the same age, based on their cranial sutures：maxillary attrition in individuals from the Jomon period（upper）, the Kofun period（middle）, and the Kamakura period（lower）. There are differences among individuals but as the period becomes closer to the present day, attrition clearly decreased. Since occlusal pits and fissures are common sites for dental caries, reduction in attrition was considered to increase the incidence of occlusal dental caries. By the Edo period, many elderly individuals can be found among skeletal remains and root dental caries and periodontal disease were found in these individuals. In addition, occlusal dental caries was also seen in the Edo people due to the reduction of attrition, while such dental caries was almost unseen in the Jomon people. Occlusal dental caries, which created a large carious cavity on the occlusal surface, was also seen in the Edo people. 5 ．The more elderly, the higher the dental caries rates among the Edo people Table 2 shows comparisons of dental caries rates in
111 Table 2 Compared of dental caries rate from the two age groups in Edo people in Japan Site
Early middle age （％）
Nagoya−City Shibashirogane Suzugamori Ubayama Ryusenji Ueno High School En−ouji Jishoin Yushima 4 chome Edo total
24.3 6.4 4.2 0.0 4.0 11.4 10.4 0.0 4.4 7.0
Elderly Total （％） （％） 33.3 4.2 11.5 11.9 18.9 18.7 17.6 16.2 32.4 18.8
30.0 6.1 8.0 6.3 12.4 16.0 13.0 9.1 8.0 12.1
Data were cited Fujita and Hirano8）
Fig. 7 Degree of dental attrition in the Jomon（upper） , Kofun（middle）and Kamakura（lower）dentitions, in Japan （IDNO：130196 from Hobi site, Yamanoue Kofun and Kamakura 103, respectively. All of them are housed in the University Museum, the University of Tokyo） .
the Edo people, who were divided into early middle age（approximately ＜39 years old）and the elderly（＞ 40 years old）. There may be some objections to categorizing ＞40 years old as elderly；however, when estimating that the average life span during the Edo period was approximately 20 years, there is some validity in placing late middle−aged people and the
elderly of ＞40 years old in the advanced age group. In this table, the dental caries rates in elderly individuals exceeded those in early middle−aged individuals for all ancient remains excavated from the archeological sites of the Edo period, except for those from the Shiba Shirogane site in Tokyo. Our study is the only one to examine dental caries rates by the age groups of ancient skeletal remains8）. The results of this study indicated that dental caries rates tended to increase with age, since the dental caries rates were higher in the elderly than in middle−aged individuals, at least in the Edo period in Japan. Even though teeth were brushed and these were denture makers during the Edo period, there was no modern treatment； therefore, dental caries occurred at relatively high rates. In addition, since dental caries progressed without treatment, older individuals would have more carious teeth. Subsequent to such comparisons of caries rates between early and late middle−aged people, Oyamada et al. conducted research on the differences in dental caries rates by class of Edo people22）. They found that the samurai warrior class had fewer dental caries than common people, and they are investigating oral hygiene and dietary habits as the cause. It is significant that caries research is evolving from mere comparisons of dental caries rates to studies based on more detailed epidemiological factors. Following is a discussion on the differences in dental caries rates among archeological sites. There are
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archeological sites in which the number of excavated individuals is small；however, it is speculated that such dental caries rate differences among these sites are created mainly by differences in dietary habits and hygiene practices；that is, the factor is the difference in class among people of that time, including the samurai, merchants, and farmers. Remains from the Edo period were excavated from the Oterayama site
Fig. 8 Excessive abrasion in the Edo dentition, Japan The abrasion must be caused by bad tooth brushing （IDNO：Ueno Senior High School Ikougai 1, from Ueno Senior High School site, and housed in the National Science Museum, Tokyo, Japan） .
and had very low dental caries rates23）. In Edo prefecture, cariogenic foods, such as sweets, were available to commoners；however, such luxury items were speculated to be unavailable in rural towns. Compared with commoners, upper class people are speculated to have had better hygiene practices, such as tooth brushing；however, many carious lesions were found in the remains of the Tokugawa shoguns. It is necessary to further examine the dietary habits and hygiene practices by class of Edo people with the cooperation of historians. Figure 8 shows a very interesting photograph, although it is slightly off topic, of an abnormal labial abrasion in an individual from the Edo period. The abnormal abrasion occurred only on the labial side and not on the lingual side as shown in the photograph. The practice of tooth brushing seemed to have been well established even among the commoners by the Edo period. This type of abrasion was thought to have occurred due to tooth brushing using tufted toothpicks or poor−quality abrasive powder. Figure 9 is a plot of carious sites in Japanese from the Jomon period to the modern day. This figure indicates a few very interesting facts. First, the percentage of dental caries on the occlusal surface is almost the same among people in the modern day, the Kama-
Fig. 9 Distribution of caries cavities（site）in each period in Japan
113
kura period, and the Edo period. The percentages are low for the Jomon and Kofun periods. As indicated previously for Fig. 6, the occurrence of occlusal dental caries was thought to have been inhibited in the period when attrition was considerable. In general, interproximal root dental caries was prevalent in all periods. It can be said that interproximal root dental caries is the most characteristic dental caries in Japanese if dental caries from all periods are examined. The incidence of lingual dental caries and lingual root dental caries was low in all periods, which can be explained by the self−cleansing action of the tongue. Conclusion In Japan, studies of caries date back to the Meiji period, and thereafter, Sakura and Inoue et al. were involved in caries research of ancient human skeletal remains3,4）．In recent years, our research group and the research groups of Oyamada et al.22,24）and Haraga et al.21）have been the leaders in caries research of ancient human skeletal remains. Time periods are truly borderless. No one knows which area will be useful in our own research area and we must therefore be attentive to research in other areas. The hope is that anthropological results from ancient human remains can be utilized to create a new vision of dental hygiene and public health in the 21st century. It is necessary to learn about the present to foresee the future；however, much can also be learned from various aspects of our ancestors. References 1）Robinson, J. T.：Some hominid features of the ape− man dentition. J. Dent. Assoc. Series Africa 7：102― 107, 1952. 2）Fujita, H.：Geographical and chronological differences in dental caries in the neolithic Jomon period of Japan. Anthropol. Sci. 103：23―37, 1995. 3）Sakura, H.：Historical change in the frequency of dental caries among the Japanese people. J. Anthropol. Soc. Nippon 71：153―177, 1964. 4）Inoue, N., Ching, H. K., Ito, G. and Kamegai, T.： Dental diseases in Japanese skeletal remains. Ⅱ.： Later Jomon period. J. Anthropol. Soc. Nippon 89：
363―378, 1981. 5）Sanui, Y.：Anthropological researches on the teeth of the prehistoric Yayoi−ancient excavated from the Doigahama site, Yamaguchi−prefecture. Jinruigaku Kenkyu 7：861―884, 1960（in Japanese）. 6）Ono, A.：Anthropological studies on the teeth of the Yayoi−age men from Mitsu, Kanzaki−gun, Saga− prefecture. Jinruigaku Kenkyu 4：423―462, 1957 （in Japanese） . 7）Inoue, N., Kuo, C. H., Ito, G. and Kamegai, T.：Dental diseases in Japanese skeletal remainⅢ, Kofun period. J. Anthrop. Soc. Nippon 89：419―426, 1981. 8）Fujita, H. and Hirano, H.：Dental caries in older adults in the Edo period, Japan. Jpn. J. Gerodontol. 13：175―182, 1999. 9）Turner, C. G. Ⅱ：Dental anthropological indications of agriculture among the Jomon people of central Japan. Am. J. Phys. Anthropol. 51：619―636, 1979. 10）Suzuki, K.：Foods sources of Jomon period. In：Japanese archaeology for studying （eds. Ohtsuka, H., Tozawa, M. and Sahara, M.） , pp.199―207, Yuhikaku, Inc. Tokyo, 1979. 11）Nishida, M.：Foods and subsistence in Jomon period. Archaeology Quarterly 11：3―41, 1980. 12）Minagawa, M.：The degree of gourmet inspected from the skeletal remains in Jomon people. In：Asahi One Theme Magazine. （ed. Miyamoto, M.） , pp.205― 211, Asahi Shimbun Inc. Tokyo, 1993. 13）Morimoto, K.：Dental caries found in Sakhalin Ainu. Mitteilungen Ame Dem Anat. Inst. Der Kaiserlichen Univ. 5：1―20, 1938. 14）Fujita, H.：Historical change of dental carious lesions from prehistoric to modern times in Japan. Jpn. J. Oral Biol. 44：87―95, 2002. 15）Moore, W. J. and Corbett, M. E.：The distribution of dental caries in ancient British populations. Ⅱ. Iron age, Romano−British and mediaeval periods. Caries Res. 7：139―153, 1973. 16）Moore, W. J. and Corbett, M. E.：The distribution of dental caries in ancient British populations. Ⅲ. The 17th century. Caries Res. 10：401―414, 1976. 17）Whittaker, D. K., Molleson, T., Bennett, R. B., Edwards, I., Jenkins, P. R. and Llewelyn, J. K.：The prevalence and distribution of dental caries in a Romano−British population. Arch. Oral Biol. 26：237 ―245, 1981. 18）Lunt, D. A.：The prevalence of dental caries in the permanent dentition of Scottish prehistoric and mediaeval populations. Arch. Oral Biol. 19：431―437,
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1974. 19）Kubota, K., Yonemitsu, M., Hollist, M. O., Ono, Y., O., Ohnishi, M., Watanabe, Nakata, M., Ajayi−Obe, S. H. and Grillo, A. I.：Five−yaer follow−up caries study among Nigerian children. Community Dent. Oral Epidemiol. 18：197―199, 1990. 20）Kobayashi, K.：Trend in the length of life based on human skeleton from prehistoric to modern times in Japan. J. Faculty Sci., the Univ. of Tokyo（V）3（2）： 107―162, 1967. 21）Haraga, S., Hamasaki, T., Ansai, T., Kakuta, S., Akifusa, S., Yoshida, A., Hanada, N., Miyazaki, H. and Takehara, T.：Distribution and site characteristics of dental caries in paddy rice−cultivating Yayoi people of
ancient Japan. J. Dent. Hlth. 56：71―78, 2006. 22）Oyamada, J., Kitagawa, Y., Manabe, Y. and Rokutanda, A.：Dental pathology in the samurai and commoners of early modern Japan. Anthropol. Sci. 112：235 ―246, 2004. 23）Sakura, H.：Low incidence of dental caries among a rural population in the early modern age unearthed from Oterayama site. Bull. Natn. Sci. Mus., Tokyo. Series D, 11：1―5, 1989. 24）Oyamada, J., Igawa, K., Kitagawa, Y., Manabe, Y., Kato, K. Matsushita, T. and Rokutanda, A：Low AMTL ratios in dmedieval Japanese dentition excavated from the Yuigahama−minami site in Kamakura. Anthropol. Sci. 115：47―53, 2007.
REVIEW
Dental Caries in Japanese Human Skeletal Remains Hisashi Fujita§ Department of Anthropology, Niigata College of Nursing, 240 Shinnan−cho, Joetsu 943−0147, Niigata, Japan 〔Received on October 14, 2008；Accepted on March 8, 2009〕 Key words：dental caries／human skeletal remains／Japanese／anthropology／palaeopathology Abstract：The focus of the present study was dental carious sites in ancient Japanese skeletal remains, which has long been a focus of research. This topic is of interest because it has not received much attention. In addition, the causes of numerous incidents of root caries observed in the investigation of dental caries in ancient skeletal remains need to be examined. The results of this study indicated that there are more root caries than coronal caries in modern−day people. In Japanese people of the Edo period or earlier, the great majority of dental carious sites were on root surfaces. The cause was the loss of alveolar bone due to periodontal disease, and the cementum of the root was exposed, resulting in caries invasion of the exposed area. This sequence of events led to a pattern of dental caries and root caries in ancient Japanese people. This type of caries can be said to be of the elderly−type caries of the modern era. It is generally speculated that the advancement of physiological aging in ancient people was very rapid as they were under considerable physical stress. Unlike modern−day people, ancient people were unable to receive scientific dental treatment, and dental caries and periodontal disease were more frequent than expected. Using information gathered from investigations over many years, the historical changes in dental caries and the characteristics of dental caries in Japanese people from the Jomon period to the modern era are outlined.
Introduction Dental caries is one of the most common human “diseases”, along with the common cold. Signs of dental caries have been seen even in the early hominids, Australopithecine1）. Dental caries can be said to be a disease that has shared its path with human evolution. In anthropology, which deals with ancient human skeletal remains, the subjects of research include dental caries as well as enamel hypoplasia, dental attrition, and periodontal diseases. These diseases are a type of stress marker and are thought to be useful to §
Corresponding author E−mail：hfujita@niigata−cn.ac.jp
understand the oral hygiene conditions of ancient peoples and to reconstruct their biological and sociological backgrounds, which could be speculated from such conditions. In particular, numerous research papers on dental caries in anthropology deal with ancient human skeletal remains, and dental caries is the disease which draws the most interest. Dental caries comprises the most case reports in dental paleopathology because the teeth are the hardest tissue in the human body；therefore, even if ancient human skeletal remains are excavated in poorly preserved conditions, dental caries can be distinguished relatively easily and data can be accumulated for statistical analysis. Furthermore, an examination of dental caries enables speculation on various epidemiological factors of the time when these ancient people lived,
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including their oral hygiene, diet, and livelihood. As is commonly known, humans have undergone an evolutionary process from early hominids, Homo erectus, Neanderthal man or Homo heidelbergensis, to moderns humans（Cro−Magnon man and onward）. Unfortunately, fossilized human bones earlier than those of Homo heidelbergensis have not been found in Japan. Even modern human bones from the Pleistocene epoch are rare；therefore, human skeletal remains, including dental caries, that can be analyzed and statistically examined as a collection or“group” are from the Jomon period and onward2）. There are two methods of researching the diseases of our ancestors, and they are not restricted to dental caries research. One method is the study of medical history. This study is mainly on pathologies in ancient documents and literature and identification of the diseases. The second method is paleopathology, a field of study in physical anthropology. In this field, the study materials are archeologically excavated hard tissues, such as bones and teeth of people from ancient times. Of course the soft tissues have long ago decayed and returned to the soil；therefore, paleopathology allows the examination of the true pathological states of certain diseases at the time of death and the prevalence of the disease among certain groups of people. Sakura and Inoue et al. reported in their research changes in the dental caries rate using ancient human skeletal remains from Japan3,4）. Their studies were outstanding for that time, but the focus was on dental caries rates；therefore, the human aspects of the ancient people of the time could not be ascertained very well. As in medical history, the basis of paleopathology is the elucidation of disease and pathological states in ancient skeletal remains. In addition, it delves deeper to investigate the structure of disease at that time and to speculate on their society based on the structure of disease. Furthermore, paleopathology has great significance in probing various sociological and biological factors, including the diet, life span, childbirth, nutrition, and hygiene of the people. This paper investigated sociological and biological factors of different periods in Japan by following the changes in dental caries. It is based on studies focus-
ing on carious sites. Descriptions 1 ．High rate of dental caries in the Jomon people Study of the teeth of the Jomon people showed a surprisingly high prevalence of dental caries, although lower than that of the general modern population. When the dental caries rates of the Jomon people were compared to those from other societies of hunters and gatherers, people from other societies generally had lower dental caries rates2）. Table 1 shows the dental caries rates of people in similar stages of hunter and gatherer societies as the Jomon people and the historical changes of dental caries rates in Japan2,5―9）. The dental caries rates were much higher in the Jomon people than even the present day Inuits of Greenland or aborigines of Australia2,9）, and unlike any other hunter and gatherer societies in the world. Most hunters and gatherers who do not farm have very low dental caries rates. When their economy transitions from hunting and gathering to farming, the incidence of dental caries is known to increase sharply. In Japan, the dental caries rates increased sharply in the Yayoi people who adopted farming2,5,6）. The high dental caries rates in the Jomon people were thought to demonstrate the intake of large amounts of high starch foods which facilitated dental caries occurrence. In addition, they probably used food preparation methods that facilitated dental caries occurrence. 2 ．Importance of plant−based food Previously, people tended to think that hunters and gatherers consumed animal−based foods more frequently than plant−based foods but the proportion of plant−based foods that hunters and gatherers consumed relative to their overall diet was larger than imagined. This result is based on recent archeological findings and ethnological surveys from various foreign countries, and it is widely accepted today. Suzuki studied the food remains of the Jomon period and reported that nuts and wild tubers were very important as plant−based sources from the view-
107 Table 1 Dental caries rate of different economies and populations in the world Groups
Age
Economic level
Caries rate（％）& Source
Jomon（Japan） Yayoi（Doigahama, Japan） Yayoi（Mitsu, Japan） Kofun（Japan） Muromachi（Japan） Edo（Japan） Old Copper（USA） SJO−68（USA） Australian Aborigine（Australia） Inuits（Denmark） Inuits（USA）
12,000―2,300 yrs BP 2,000 yrs BP 2,000 yrs BP ca. AD 1700―1400 yrs ca. AD 1400 yrs AD 1603―1868 yrs 7,600 yrs BP 3,000 yrs BP Modern Modern Modern
hunting−gathering agriculture agriculture agriculture agriculture agriculture hunting−gathering hunting−gathering hunting−gathering hunting−gathering hunting−gathering & trade
8.22） 19.75） 16.26） 8.37） 14.63） 12.18） 0.49） 2.49） 4.69） 2.29） 1.99）
Caries rate（％） ：100（carious teeth／teeth present）
point of both calories and degree of edibility10）. He also indicated that the harvest times of fruits, leaves, and stalks were staggered, showing good distribution by season. Nishida studied the Torihama shell mound and reported that the largest proportion of total calories （43％）came from nuts, such as walnuts and acorns, followed by fish and meat11）. The most abundant food remains are of shellfish, which has relatively low calories. Thus, it was speculated that the main diet of the shell mound people along the coast consisted of plant−based foods. Minagawa conducted a very interesting study that investigated the diet of Jomon people by stable isotope analysis. He stated that the Jomon people probably consumed large amounts of plant−based foods. He believed that the Ainus in Hokkaido at that time consumed large amounts of animal−based food, unlike the Jomon people on Honshu12）. In actuality, the modern−day Ainus surveyed during the Edo, Meiji, and Taisho periods had a great preference for animal− based foods13）. It was reported that they even consumed the internal organs of the animals. This is very suggestive when considering that dental caries ；therefore, one prevalence is very low in the Ainus13） reason for the high dental caries rates in the Jomon people can be found in their diet, which was mainly plant−based foods.
3 ．Elderly−type dental caries in modern day Dental caries in the Jomon people can be compared with that in modern−day people. The present study focused on the sites of dental caries occurrence. The most common sites of dental caries are occlusal and interproximal areas in modern−day people, whereas the Jomon people were more likely to have dental caries in the interproximal areas, buccal cervical areas, and root areas （Fig. 1）, occlusal dental caries was 14） rare . The pattern of carious sites in the Jomon people is very similar to that in the modern−day elderly. The direct cause is exposure of the cervical and root areas due to the recession of gingiva and alveolar bone. Crowns are covered by enamel but cervical and root areas are composed of cementum；therefore, these areas are structurally weaker against the invasion of dental caries. Figure 2 is the oral image of a man in his 70s who presented at the Department of Dental Oral Surgery of the Tokyo Metropolitan Geriatric Hospital. His gingiva was inflamed, and his alveolar bone was receded. Unlike the Jomon people, this patient did not have buccal dental caries, probably due to the effect of brushing；however, the occurrence of root dental caries due to alveolar bone loss was determined to be almost the same as in the Jomon people； therefore, the pattern of dental caries in the Jomon people was similar to elderly−type dental caries in the modern day.
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Fig. 1 Root caries in the Japanese Jomon people（IDNO：131638 from Tsugumo site, and is housed in the University Museum, the University of Tokyo, Japan） .
Fig. 2 Root caries in the modern elderly people in Japan （This photograph is housed in the Department of Oral Surgery, Tokyo Metoropolitan Geriatric Hospital, Japan）.
Interestingly, researchers from various countries obtained similar results regarding cariaus sites in ancient man. Moore, Corbett, and Whittaker et al. studied dental caries in the ancient English15―17） and Lunt studied dental caries from prehistoric times and the Middle Ages in Scottish populations18）. All of these researchers indicated a high incidence of cervical and root dental caries. Two main factors explaining the above results can
Fig. 3 Occlusal dental caries in the Japanese Jomon people （young individual, IDNO：Satohama 15 from Satohama site, and is housed in the National Science Museum, Tokyo, Japan）.
be suggested. First, the progress of attrition was incomparably fast in people in ancient times and the Middle Ages relative to modern−day people. If dental caries in the occlusal pits and fissures was mild, the progression of attrition could have been faster than that of such dental caries；therefore, it is presumed that dental caries itself could have disappeared in many cases. This phenomenon is seen in modern Nigeria. Kubota et al. conducted follow−up surveys of people in Nigeria with dental diseases19）. Figure 3 shows occlusal dental caries in the Jomon people. Although the prevalence of occlusal dental caries was low in the Jomon period, it certainly did exist. Cusps and fissures were well preserved on this individual’s occlusal surfaces. An anthropologist familiar with the bones and teeth of ancient skeletal remains can easily determine that the individual was rather young；that is, such an individual with well− preserved cusps and fissures could have occlusal dental caries. The Jomon people were eating food much harder than that of modern−day people；therefore, their attrition was considerable. Occlusal dental caries was presumed not to have occurred in an individual with occlusal surfaces, such as those shown in Fig. 4. In other words, occlusal dental caries could be found in young people, but it became less likely in individuals beyond a certain age as attrition progressed with aging. If attrition was very considerable, mild occlusal
109
Fig. 4 Severe dental attrition in the Japanese Jomon people （IDNO：130196 from Hobi site, and is housed in the University Museum, the University of Tokyo, Japan） .
Fig. 5 Pulp exposure caused of severe attrition in the Japanese Jomon people （IDNO：Hikozaki 6 from Hikozaki site, and housed in the National Science Museum, Tokyo, Japan）.
dental caries could have disappeared due to attrition, as in the aforementioned Nigerian cases. The causes of marked attrition of the Jomon people are probably also found in factors other than diet. As shown in Fig. 5, attrition of the anterior teeth could have occurred due to the use of teeth for hide tanning, just as in Inuits. It was speculated that teeth were used as“tools”. In this individual, the pulp cavities were exposed, and they were in a state of pulp exposure. Even if the Jomon people ate hard food, factors other than diet must be considered to explain the extreme attrition. The second reason for the high incidence of root dental caries is periodontal disease, which was speculated to have occurred at a very high frequency. Many excavated Jomon individuals had advanced alveolar bone resorption. As in modern−day people, bone resorption due to periodontal disease was seen in the Jomon people. The incidence of periodontal disease is closely associated with aging；therefore, a brief statement is provided below regarding aging and life span of the Jomon people. The average life span of the Jomon people has been provisionally calculated at approximately under 15 years for both males and females20）. This short life span was due to the remarkably high infant mortality rate, which reduced the overall life span of people in
the Jomon period. In anthropology, when studying a group with an extremely short life span, focus is placed on the average life expectancy of the 15−year− old survivors. This is an age at which a person gains some degree of resistance to disease. In the Jomon individuals who survived the first 15 years of life, the life expectancy was considered to be approximately an additional 15 years；that is, the average life span of such individuals was approximately 30 years. Even if some individuals had a life span longer than 30 years, the resorption of alveolar bone in the Jomon people was speculated to be 20―30 years faster than in modern−day people. This suggests that the Jomon people aged considerably faster than modern−day people and that periodontal disease was very common in a period without special measures for disease prevention and treatment. 4 ．Root dental caries is“ancient−type dental caries” As mentioned previously, dental caries in the Jomon people were found on the root surfaces in many cases, associated with loss of alveolar bone with periodontal disease and aging, and root dental caries in the modern’s elderly is similar to dental caries in the Jomon people. As shown in Fig. 1, root dental caries tended to be more prevalent than coronal
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Fig. 6 Occlusal dental caries in the Japanese Edo people（IDNO：Suzugamori M2 from Suzugamori site, and housed in the National Science Museum, Tokyo, Japan） .
dental caries in all time periods in Japan when human bones were examined from these periods.（There was no significant difference between the Jomon and Kamakura periods. When more materials are collected, a statistically significant difference could be indicated between these periods）. The incidence of coronal dental caries is significantly large only in modern−day people；therefore, root dental caries can be considered as“ancient−type dental caries.”Haraga et al. examined caries in Yayoi human skeletal remains excavated in northern Kyushu and found a high percentage of root caries in these remains. Their result is important as it is consistent with our findings21）. If there are many elderly individuals among the examined human bones, then the proportion of root dental caries is predicted to increase. If there are many young individuals, the proportion of coronal dental caries is predicted to increase. Human skeletal remains of the Kamakura period were excavated from the Zaimokuza site in Kamakura city, Kanagawa prefecture. Many of these individuals are considered to be people who died in action during the Kamakura attack of Y. Nitta during the fall of the Kamakura shogunate；therefore, they are thought to be relatively young. If there are many young individuals, the numbers of occlusal dental caries and coronal dental caries should be high. In paleopathology, using limited
materials, it is usually difficult to match the age of people in the group and to compare them under the same conditions. Root dental caries was prevalent in the ancient people of Japan because periodontal disease was prevalent and the root was exposed when there was no scientific dental care. In addition, the progress of physiological aging was markedly faster in ancient people than in modern−day people. It has been speculated that even at a young chronological age, people had periodontal disease. Figure 6 shows the dental caries found in mandibles of people from the Edo period. Occlusal dental caries advanced directly to the root area without affecting the surroundings in the coronal portion. This type of dental caries is seen in relatively young people in the modern day. In addition, this pattern of dental caries is almost never seen in Jomon individual, who had severe attrition. As mentioned in the previous journal issue, it was probably difficult for dental caries to occur on the flat occlusal surfaces of Jomon people who had considerable attrition, and mild dental caries probably disappeared due to attrition. Figure 7 shows the images of individuals estimated to be approximately the same age, based on their cranial sutures：maxillary attrition in individuals from the Jomon period（upper）, the Kofun period（middle）, and the Kamakura period（lower）. There are differences among individuals but as the period becomes closer to the present day, attrition clearly decreased. Since occlusal pits and fissures are common sites for dental caries, reduction in attrition was considered to increase the incidence of occlusal dental caries. By the Edo period, many elderly individuals can be found among skeletal remains and root dental caries and periodontal disease were found in these individuals. In addition, occlusal dental caries was also seen in the Edo people due to the reduction of attrition, while such dental caries was almost unseen in the Jomon people. Occlusal dental caries, which created a large carious cavity on the occlusal surface, was also seen in the Edo people. 5 ．The more elderly, the higher the dental caries rates among the Edo people Table 2 shows comparisons of dental caries rates in
111 Table 2 Compared of dental caries rate from the two age groups in Edo people in Japan Site
Early middle age （％）
Nagoya−City Shibashirogane Suzugamori Ubayama Ryusenji Ueno High School En−ouji Jishoin Yushima 4 chome Edo total
24.3 6.4 4.2 0.0 4.0 11.4 10.4 0.0 4.4 7.0
Elderly Total （％） （％） 33.3 4.2 11.5 11.9 18.9 18.7 17.6 16.2 32.4 18.8
30.0 6.1 8.0 6.3 12.4 16.0 13.0 9.1 8.0 12.1
Data were cited Fujita and Hirano8）
Fig. 7 Degree of dental attrition in the Jomon（upper） , Kofun（middle）and Kamakura（lower）dentitions, in Japan （IDNO：130196 from Hobi site, Yamanoue Kofun and Kamakura 103, respectively. All of them are housed in the University Museum, the University of Tokyo） .
the Edo people, who were divided into early middle age（approximately ＜39 years old）and the elderly（＞ 40 years old）. There may be some objections to categorizing ＞40 years old as elderly；however, when estimating that the average life span during the Edo period was approximately 20 years, there is some validity in placing late middle−aged people and the
elderly of ＞40 years old in the advanced age group. In this table, the dental caries rates in elderly individuals exceeded those in early middle−aged individuals for all ancient remains excavated from the archeological sites of the Edo period, except for those from the Shiba Shirogane site in Tokyo. Our study is the only one to examine dental caries rates by the age groups of ancient skeletal remains8）. The results of this study indicated that dental caries rates tended to increase with age, since the dental caries rates were higher in the elderly than in middle−aged individuals, at least in the Edo period in Japan. Even though teeth were brushed and these were denture makers during the Edo period, there was no modern treatment； therefore, dental caries occurred at relatively high rates. In addition, since dental caries progressed without treatment, older individuals would have more carious teeth. Subsequent to such comparisons of caries rates between early and late middle−aged people, Oyamada et al. conducted research on the differences in dental caries rates by class of Edo people22）. They found that the samurai warrior class had fewer dental caries than common people, and they are investigating oral hygiene and dietary habits as the cause. It is significant that caries research is evolving from mere comparisons of dental caries rates to studies based on more detailed epidemiological factors. Following is a discussion on the differences in dental caries rates among archeological sites. There are
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archeological sites in which the number of excavated individuals is small；however, it is speculated that such dental caries rate differences among these sites are created mainly by differences in dietary habits and hygiene practices；that is, the factor is the difference in class among people of that time, including the samurai, merchants, and farmers. Remains from the Edo period were excavated from the Oterayama site
Fig. 8 Excessive abrasion in the Edo dentition, Japan The abrasion must be caused by bad tooth brushing （IDNO：Ueno Senior High School Ikougai 1, from Ueno Senior High School site, and housed in the National Science Museum, Tokyo, Japan） .
and had very low dental caries rates23）. In Edo prefecture, cariogenic foods, such as sweets, were available to commoners；however, such luxury items were speculated to be unavailable in rural towns. Compared with commoners, upper class people are speculated to have had better hygiene practices, such as tooth brushing；however, many carious lesions were found in the remains of the Tokugawa shoguns. It is necessary to further examine the dietary habits and hygiene practices by class of Edo people with the cooperation of historians. Figure 8 shows a very interesting photograph, although it is slightly off topic, of an abnormal labial abrasion in an individual from the Edo period. The abnormal abrasion occurred only on the labial side and not on the lingual side as shown in the photograph. The practice of tooth brushing seemed to have been well established even among the commoners by the Edo period. This type of abrasion was thought to have occurred due to tooth brushing using tufted toothpicks or poor−quality abrasive powder. Figure 9 is a plot of carious sites in Japanese from the Jomon period to the modern day. This figure indicates a few very interesting facts. First, the percentage of dental caries on the occlusal surface is almost the same among people in the modern day, the Kama-
Fig. 9 Distribution of caries cavities（site）in each period in Japan
113
kura period, and the Edo period. The percentages are low for the Jomon and Kofun periods. As indicated previously for Fig. 6, the occurrence of occlusal dental caries was thought to have been inhibited in the period when attrition was considerable. In general, interproximal root dental caries was prevalent in all periods. It can be said that interproximal root dental caries is the most characteristic dental caries in Japanese if dental caries from all periods are examined. The incidence of lingual dental caries and lingual root dental caries was low in all periods, which can be explained by the self−cleansing action of the tongue. Conclusion In Japan, studies of caries date back to the Meiji period, and thereafter, Sakura and Inoue et al. were involved in caries research of ancient human skeletal remains3,4）．In recent years, our research group and the research groups of Oyamada et al.22,24）and Haraga et al.21）have been the leaders in caries research of ancient human skeletal remains. Time periods are truly borderless. No one knows which area will be useful in our own research area and we must therefore be attentive to research in other areas. The hope is that anthropological results from ancient human remains can be utilized to create a new vision of dental hygiene and public health in the 21st century. It is necessary to learn about the present to foresee the future；however, much can also be learned from various aspects of our ancestors. References 1）Robinson, J. T.：Some hominid features of the ape− man dentition. J. Dent. Assoc. Series Africa 7：102― 107, 1952. 2）Fujita, H.：Geographical and chronological differences in dental caries in the neolithic Jomon period of Japan. Anthropol. Sci. 103：23―37, 1995. 3）Sakura, H.：Historical change in the frequency of dental caries among the Japanese people. J. Anthropol. Soc. Nippon 71：153―177, 1964. 4）Inoue, N., Ching, H. K., Ito, G. and Kamegai, T.： Dental diseases in Japanese skeletal remains. Ⅱ.： Later Jomon period. J. Anthropol. Soc. Nippon 89：
363―378, 1981. 5）Sanui, Y.：Anthropological researches on the teeth of the prehistoric Yayoi−ancient excavated from the Doigahama site, Yamaguchi−prefecture. Jinruigaku Kenkyu 7：861―884, 1960（in Japanese）. 6）Ono, A.：Anthropological studies on the teeth of the Yayoi−age men from Mitsu, Kanzaki−gun, Saga− prefecture. Jinruigaku Kenkyu 4：423―462, 1957 （in Japanese） . 7）Inoue, N., Kuo, C. H., Ito, G. and Kamegai, T.：Dental diseases in Japanese skeletal remainⅢ, Kofun period. J. Anthrop. Soc. Nippon 89：419―426, 1981. 8）Fujita, H. and Hirano, H.：Dental caries in older adults in the Edo period, Japan. Jpn. J. Gerodontol. 13：175―182, 1999. 9）Turner, C. G. Ⅱ：Dental anthropological indications of agriculture among the Jomon people of central Japan. Am. J. Phys. Anthropol. 51：619―636, 1979. 10）Suzuki, K.：Foods sources of Jomon period. In：Japanese archaeology for studying （eds. Ohtsuka, H., Tozawa, M. and Sahara, M.） , pp.199―207, Yuhikaku, Inc. Tokyo, 1979. 11）Nishida, M.：Foods and subsistence in Jomon period. Archaeology Quarterly 11：3―41, 1980. 12）Minagawa, M.：The degree of gourmet inspected from the skeletal remains in Jomon people. In：Asahi One Theme Magazine. （ed. Miyamoto, M.） , pp.205― 211, Asahi Shimbun Inc. Tokyo, 1993. 13）Morimoto, K.：Dental caries found in Sakhalin Ainu. Mitteilungen Ame Dem Anat. Inst. Der Kaiserlichen Univ. 5：1―20, 1938. 14）Fujita, H.：Historical change of dental carious lesions from prehistoric to modern times in Japan. Jpn. J. Oral Biol. 44：87―95, 2002. 15）Moore, W. J. and Corbett, M. E.：The distribution of dental caries in ancient British populations. Ⅱ. Iron age, Romano−British and mediaeval periods. Caries Res. 7：139―153, 1973. 16）Moore, W. J. and Corbett, M. E.：The distribution of dental caries in ancient British populations. Ⅲ. The 17th century. Caries Res. 10：401―414, 1976. 17）Whittaker, D. K., Molleson, T., Bennett, R. B., Edwards, I., Jenkins, P. R. and Llewelyn, J. K.：The prevalence and distribution of dental caries in a Romano−British population. Arch. Oral Biol. 26：237 ―245, 1981. 18）Lunt, D. A.：The prevalence of dental caries in the permanent dentition of Scottish prehistoric and mediaeval populations. Arch. Oral Biol. 19：431―437,
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1974. 19）Kubota, K., Yonemitsu, M., Hollist, M. O., Ono, Y., O., Ohnishi, M., Watanabe, Nakata, M., Ajayi−Obe, S. H. and Grillo, A. I.：Five−yaer follow−up caries study among Nigerian children. Community Dent. Oral Epidemiol. 18：197―199, 1990. 20）Kobayashi, K.：Trend in the length of life based on human skeleton from prehistoric to modern times in Japan. J. Faculty Sci., the Univ. of Tokyo（V）3（2）： 107―162, 1967. 21）Haraga, S., Hamasaki, T., Ansai, T., Kakuta, S., Akifusa, S., Yoshida, A., Hanada, N., Miyazaki, H. and Takehara, T.：Distribution and site characteristics of dental caries in paddy rice−cultivating Yayoi people of
ancient Japan. J. Dent. Hlth. 56：71―78, 2006. 22）Oyamada, J., Kitagawa, Y., Manabe, Y. and Rokutanda, A.：Dental pathology in the samurai and commoners of early modern Japan. Anthropol. Sci. 112：235 ―246, 2004. 23）Sakura, H.：Low incidence of dental caries among a rural population in the early modern age unearthed from Oterayama site. Bull. Natn. Sci. Mus., Tokyo. Series D, 11：1―5, 1989. 24）Oyamada, J., Igawa, K., Kitagawa, Y., Manabe, Y., Kato, K. Matsushita, T. and Rokutanda, A：Low AMTL ratios in dmedieval Japanese dentition excavated from the Yuigahama−minami site in Kamakura. Anthropol. Sci. 115：47―53, 2007.