Anthropological Science
Online ISSN : 1348-8570
Print ISSN : 0918-7960
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Original Articles
Sex differences in linear enamel hypoplasia (LEH) in early modern Japan
JOICHI OYAMADAYOSHIKAZU KITAGAWAKATSUTOMO KATOTAKAYUKI MATSUSHITATOSHIYUKI TSURUMOTOYOSHITAKA MANABE
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2012 Volume 120 Issue 2 Pages 97-101

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Abstract

In Japan’s early modern period (1603–1867), also known as the Edo period, females were considered inferior to males. It is therefore plausible that boys were raised more solicitously than girls, and that girls were subject to various kinds of deprivation in early childhood. We compared the prevalence of linear enamel hypoplasia (LEH) in the dentition of the skeletal remains of early modern Japanese samurai and commoners interred in an urban location (a castle town). Significant sex differences were found in the prevalence of LEH in both groups. As there is evidence that LEH prevalence reflects stress levels in early childhood, the significant differences between the sexes provide material evidence for the hypothesis that male offspring were given preferential treatment among both samurai and commoners in Edo period urban society.

Introduction

During the early modern period in Japan (1603–1867), also known as the Edo period, a class system divided the population by law into samurai, farmers, craftsmen, and merchants. Under this feudal system, and especially within samurai society, females were considered inferior to males. In his 1710 educational book Wazoku-douzikunn (revised by Ishikawa, 1961), Ekiken Kaibara, a famous Edo period Confucianist, stated that a woman should serve her father before marriage, her husband after marriage, and her children after the death of her husband. It was customary that a “seven-year-old female should not share a seat with a male,” and giving birth to a male heir was considered a bride’s obligation—“if there is not a child after three years of marriage, the bride should leave” (Research Project on the Lives of Samurai, 1991). It seems likely that in a society with these values, boys would be favored in child-rearing practices, including those impacting nutrition.

Studies of human bone pathology have identified linear enamel hypoplasia (LEH), cribra orbitalia, and Harris’ line as stress markers in human growth. As LEH occurs during tooth formation, the teeth involved indicate the age at which stress occurred, making LEH a valuable developmental stress marker. In a society that favors males, one might expect to find more evidence of stress in the teeth of females than of males, indicating the preferential treatment of males in child-rearing.

Yamamoto (1988) found the highest prevalence of LEH in the permanent teeth of early modern skeletal remains in the lower canines, followed by the upper central incisors and lower lateral incisors. In our previous study of early modern commoners in urban and rural areas (Oyamada et al., 2010), we found the highest prevalence of LEH in the lower canines.

In the present study, teeth in the skeletal remains of early modern samurai and commoners from an urban area (a castle town) were examined for differences between the sexes in the prevalence of LEH, which would lend support to the hypothesis of preferential treatment of males in child-rearing practices.

Materials and Methods

The historic site of Sougenji Temple, in Kokura, Fukuoka Prefecture is also a burial ground (Figure 1). In the early modern period, Kokura was a castle town ruled by the Ogasawara family. Sougenji Temple was initially founded by Ogasawara Hidemasa, lord of Shinshu Matsumoto, in Shinshu Matsumoto in the district of Chubu. However, the temple was moved when the Ogasawara family was transferred by the Edo Shogunate to Kokura, Kyushu in 1632. The temple burned down in 1866, but was rebuilt in 1869. The current temple was rebuilt in its present location in 1975.

Figure 1

Map of the sites discussed in the present study.

The historic site was excavated in 1992. Over 600 graves were revealed, containing 357 skeletons of Ogasawara retainers belonging to the samurai class. From archeological evidence, such as the form and design of vessels, it has been estimated that the bodies were buried during the 17th or 18th centuries (Ogata, 1995).

The Kyoumachi burial site is also in an urban area in Kokura, Fukuoka Prefecture, near the Sougenji Temple site. This site was also excavated in 1992, and 1211 skeletons of commoners, including members of the farmer and merchant classes, were unearthed. Archeologists have estimated that they were buried during the 16th–19th centuries (Kamimura, 1993).

The lower canines, upper central incisors, and lower lateral incisors were chosen for examination, as these teeth were previously found to be most affected by LEH in the early modern Japanese population (Yamamoto, 1988). To eliminate observer bias, one of the authors (T.M.) judged the sex of each individual from skeletal morphology, and the first author (J.O.) examined the remains for LEH and recorded the results.

For the purposes of sex estimation, only adult remains (16 years and over) were included in the study. None of the teeth required exclusion from the study because of severe attrition (i.e. over half of the tooth crown height missing).

Results

Influence of tooth brushing

As the target teeth of the present study (lower canines, lateral incisors and upper central incisors) are particularly susceptible to erosion by tooth brushing, we already had been examined for evidence of tooth brushing was analyzed by class (Oyamada et al., 2004). Over 20% of the dental remains of samurai at the site showed evidence of tooth brushing, compared with only 2.7% of commoners.

The incidence of LEH was analyzed by sex independently for the samurai and commoner groups. The numbers of skeletons with LEH by tooth type and by sex among the samurai with polished teeth and without polished teeth, and among commoners, are shown in Table 1. The commoners did not include individuals with polished teeth in the present study. Line and groove LEH were observed, but pit LEH was not.

Table 1 Prevalence of linear enamel hypoplasia (LEH)
Samurai with polished teeth Male Female
Line Groove Total Observable Line Groove Total Observable
LC LEH 5 0 5 17 2 0 2 3
LEH% 29.4 0.0 29.4 66.7 0.0 66.7
UI1 LEH 2 0 2 10 0 0 0 2
LEH% 20.0 0.0 20.0 0.0 0.0 0.0
LI2 LEH 2 1 3 19 1 0 1 3
LEH% 10.5 5.3 15.8 33.3 0.0 33.3
Samurai without polished teeth Male Female
Line Groove Total Observable Line Groove Total Observable
LC LEH 14 4 18 30 30 3 33 40
LEH% 46.7 13.3 60.0 75.0 7.5 82.5
UI1 LEH 4 0 4 24 12 0 12 31
LEH% 16.7 0.0 16.7 38.7 0.0 38.7
LI2 LEH 7 2 9 20 19 0 19 36
LEH% 35.0 10.0 45.0 52.8 0.0 52.8
Commoners Male Female
Line Groove Total Observable Line Groove Total Observable
LC LEH 29 1 30 43 19 3 22 24
LEH% 67.4 2.3 69.8 79.2 12.5 91.7
UI1 LEH 9 0 9 28 15 1 16 24
LEH% 32.1 0.0 32.1 62.5 4.2 66.7
LI2 LEH 19 0 19 37 16 1 17 28
LEH% 51.4 0.0 51.4 57.1 3.6 60.7

Observable, Number of observable individuals.

U, upper; L, lower; I, incisor, C, canine.

To examine the influence of tooth polishing on LEH, chi-square tests or Fisher’s exact probability tests were performed to compare the incidence of LEH in samurai with and without polished teeth. The prevalence of groove plus line LEH in the lower canines of samurai males with polished teeth was significantly lower than that in samurai males without polished teeth (with, 29.4%; without, 60.0%; P < 0.05). The prevalence of groove plus line LEH in samurai with polished teeth was lower than that in samurai without polished teeth, except in the upper central incisors of males. As these results indicate a significant influence of tooth polishing on the incidence of LEH, samurai with polished teeth were excluded from the analysis.

Sex differences

Figure 2 shows the prevalence of LEH in the lower canines, upper central incisors, and lower lateral incisors in males and females in the samurai and commoner groups. There were no significant differences between males and females in groove LEH alone in either group (Table 2). However, when groove and line LEH were combined, a significantly higher prevalence was found in the lower canines of females than males in both the samurai (males, 60.0%; females, 82.5%) and commoner (males, 69.8%; females 91.7%) groups. Although there was a greater incidence of LEH in the upper central incisors of samurai females, the difference was not significant at the 0.05 level (males, 16.7%; females, 38.7%; χ2 = 3.19; P < 0.08); however, in commoners a significant difference was again observed (males, 32.1%; females, 66.7%). Although there were no significant differences for the lower lateral incisors, prevalence was again higher in females than males in both the samurai (males 45.0%, females 52.8%) and commoner (males 51.4%, females 60.7%) groups.

Figure 2

Prevalence of linear enamel hypoplasia (LEH). For abbreviations, see Table 1.

Table 2 Results of significant tests between sex and class
Male vs. Female Samurai vs. Commoners
Samurai Male
Groove Total Groove Total
LC *
UI1
LI2
Commoners Female
Groove Total Groove Total
LC *
UI1 * *
LI2
*  P < 0.05; —, not significant.

For abbreviations, see Table 1.

Differences between samurai and commoners

Although there is only one significant difference in the groove plus line LEH prevalence of female upper central incisor (Table 2), regarding the groove plus line LEH prevalence of both males and females in all teeth types commoners are higher than samurai (lower canines; samurai males: 60.0%, commoner males: 69.8%, samurai females: 82.5%, commoner females: 91.7%, upper central incisors; samurai males: 16.7%, commoner males: 32.1%, samurai females: 38.7%, commoner females: 66.7%, lower lateral incisors; samurai males: 45.0%, commoner males: 51.4%, samurai females: 52.8%, commoner females: 60.7%).

Discussion

Age-related origin of LEH

In general, LEH arises from disturbances to ameloblasts during enamel matrix production and a resultant deficiency in the thickness of the enamel. Causative conditions include nutritional deficiencies, endocrine disorders, and infectious diseases, primarily congenital syphilis (Ishikawa and Akiyoshi, 1978; Pindborg, 1982). Severe endemic LEH in a population can be a sign of generally poor living conditions and extreme stress during childhood (Goodman et al., 1980; Lanphear, 1990; Ubelaker, 1992; Wood, 1996; Malville, 1997).

Reid and Dean (2000) estimated that the period of tooth crown formation for the lower canines is from 1.5 to 6.2 years of age, that for the upper central incisors is from 1.0 to 5.0 years, and that for the lower lateral incisors is from 1.0 to 4.2 years. Thus, the period of formation of these three tooth types is from 1.0 to 6.2 years of age, and LEH observed in adults reflects stress suffered over the period of early childhood.

Sex differences

Beginning with Yamamoto’s (1988) study, a considerable number of similar studies of LEH in Japanese skeletal remains have been published (Yamamoto, 1989; Shigehara, 1994; Koga, 2003; Temple, 2007, 2008, 2010; Hoover and Matsumura, 2008; Oxenham and Matsumura, 2008; Sawada et al., 2008). However, an investigation of sex differences in LEH for a particular period in Japan has not previously been reported. Research in other countries has produced contradictory results: higher prevalence in males (Van Gerven, et al., 1990; Saunders and Keenleyside, 1999; Palubeckaite, et al., 2002), higher prevalence in females (May et al., 1993; Slaus, 2000; King, et al., 2005), and no significant differences between the sexes (Goodman et al., 1980; Lanphear, 1990; Duray, 1996; Malville, 1997; Lovell and Whyte, 1999; Slaus, 2008).

Sex differences in the prevalence of LEH have been attributed to various factors, including sex differences in susceptibility to stress and discriminatory allocation of nutritional and medical resources in favor of male offspring. Studies of living children have shown that differential treatment of males and females in childhood can predict differences in levels of LEH in adulthood (May et al., 1993). Moreover, from the investigation of enamel hypoplasia in deciduous and permanent dentition of human and non-human primates, Guatelli-Steinberg and Lukacs (1999) insisted that though females are better buffered against environmental stress, a weak influence of male vulnerability on the expression of enamel hypoplasia is most likely to be detected in samples of very large size (>1000 individuals), and that evidence of higher enamel hypoplasia prevalence in girls might therefore be used as a biological marker of preferential investment in sons.

In the early modern period, concern over the continuity of the lineage made the survival of a male heir of prime importance for samurai, resulting in the devaluing of female children (Research Project on the Lives of Samurai, 1991). Our study of LEH in early modern urban skeletal remains revealed a higher prevalence of LEH in samurai females than males in all three tooth types, with a significant difference observed for the lower canines. It is therefore highly likely that boys were favored in child-rearing practices and that girls consequently suffered health deficiencies, resulting in the differences between the sexes in LEH prevalence in the lower canines seen in the present study.

For commoners, there was a higher prevalence of LEH in all three tooth types, and the differences were significant for both lower lateral canines and upper central incisors. The commoners in this study were probably primarily urban farmers and urban merchants (Kamimura, 1993). It is likely that during the early modern period females were considered inferior to males among the farmer and merchant classes as well (Ishikawa, 1961; Hayashi, 1993), as a male heir was important for the continuation of the business.

Differences between samurai and commoners

Both samurai and commoners in the present study were urban dwellers. For every tooth type, the prevalence of LEH was higher among commoners than among samurai, although the difference was only significant for the upper central incisors of females. For this reason, though the difference was small, postnatal stress of commoners is thought to be severe compared to the samurai.

The present results are confined to adults who survived to adulthood (over 16 years old) in a single urban area. Future studies will investigate sex differences in LEH in rural dwellers and other urban locations.

Conclusion

The present study identified significant differences between the sexes in the prevalence of LEH in the dental remains of Edo period urban-dwelling samurai and commoners. This is in keeping with the supposition that cultural values favoring males during this period resulted in the preferential treatment of boys.

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