Difference in linear enamel hypoplasia frequency between the 16^th- to 19^th-century agrarian populations of the Korean Joseon dynasty and Siberian Russia

Abstract

We studied linear enamel hypoplasia (LEH) in cranial series representative of Eurasian farmers with divergent lifestyles and natural environments: Siberian Russian settlers and Joseon dynasty people. The teeth of Siberian settlers and Joseon people of the 16^th–19^th centuries were examined in this study. We inspected specimens to detect signs of LEH, and the intergroup prevalence was statistically compared. The proportions of LEH were compared by age and sex across each group. Statistical analysis was performed with R software. Russian settlers’ LEH incidence per individual was 4.1% (3/73), whereas that of the Joseon people was 61.5% (56/91). In the case of LEH per tooth, Russian settlers and Joseon Koreans exhibited rates of 1.9% (24/1297) and 16.8% (336/2001), respectively. The statistical difference in the incidence of LEH between the two groups was highly significant (per individual: P = 9.188 × 10^–14; per tooth: P < 2.2 × 10^–16). The prevalence of LEH was observed to be much higher in the Joseon population than in the West Siberian settlers. In conclusion, we hypothesize that East Asian people’s physiological stress in childhood was far higher than that of Russian settlers. Historical LEH frequency on the Eurasian continent was truly diverse, possibly due to divergent stress conditions affecting different groups of people.

Introduction

Linear enamel hypoplasia (LEH) is a dental sign that can be taken as a reference for estimating physiological stress in and among human populations (Goodman et al., 1988; Lewis and Robert, 1997; Novak and Slaus, 2010; Wheeler, 2012). It is caused by the temporary arrest of enamel matrix growth, probably due to any type(s) of stress during amelogenesis (Goodman and Rose, 1991). LEH formation is known to be related to poor nutrition and infectious diseases contracted during childhood (Goodman, 1991, 1992). It thus can provide useful information on the health status of children and differences among human populations in this respect (Huss-Ashmore et al., 1982; Larsen, 1997; Temple, 2010).

Historically, LEH rates vary by lifestyle (Krenz-Niedbała, 2014). According to some anthropological studies, the incidence of LEH among hunter-gatherers’ is less than among farmers (Cohen and Armelagos, 1984; Bocquet-Appel and Bar-yosef, 2008), although others dispute this (Oxenham, 2006; Douglas and Pietrusewsky, 2007; Temple, 2010). In support of the former view is the opinion that the health status of human populations generally declined rather than improved with the advent of farming in human history (Krenz-Niedbała, 2014; Tomczyk et al., 2012).

However, even after agriculture was established in history, people around the world enjoyed various lifestyles and lived in different environmental conditions. As much as the pattern of LEH changes with historical development in time, various groups may have shown different patterns of LEH expression at the same period. Reports on LEH before the 20th century, when rapid industrialization took place, are not uncommon in East Asia. Yamamoto (1989) reported rates of LEH per individual in Edo-period Japan (1603–1868 CE). Nakayama (2016) tried to reveal the association between the LEH occurrence and social status in 18^th- to 19^th-century Japanese populations. The same author also attempted to study diachronic change in LEH occurrence during the Edo period (Nakayama, 2019). Oyamada et al. (2012) revealed a difference in LEH incidence between females and males of Edo-period Japanese as well.

This notwithstanding, it remains unclear the extent to which the LEH rates of East Asian people have differed from those of other agricultural societies under various subsistence strategies, lifestyles, and natural environments. In particular, very few studies of the necessary design to minimize observer bias (one research team on two or more cranial groups) have been carried out, and thus the database on which to draw is insufficient. Most studies were conducted only on groups within East Asia, and LEH comparisons with groups outside East Asia have rarely reported in the absence of observer bias.

We therefore undertook to examine the incidence of LEH of Joseon-dynasty Korean people and compare it with that of Russian settlers in Siberia, who followed different farming strategies during the 16^th–19^th centuries. Russian settlers cannot be said to represent all people in and outside East Asia, and it is not clear why the differences between the two groups, if any, arise. However, since Russians were one of the easternmost Europeans in the Eurasian continent at that time, they provide a good opportunity for us to estimate the trends of East Asian LEH incidence compared with that among people in other regions.

Materials and Methods

We examined the 16^th- to 19^th-century cranial series representative of two Eurasian farmer groups (Figure 1). The first group, Korean crania of the Joseon-dynasty period, maintained currently at Seoul National University (Seoul, South Korea), represent 91 individuals (48 males and 43 females). The total number of teeth was 2001. All of these bones were found in Joseon-dynasty graves called hoegwakmyo. Since they were originated from a variety of social classes ranging from rich peasants to nobility (Kim et al., 2023), it is not certain that all of the people found in this tomb had the same standard of living. However, considering that the graves were built for middle-class people and above, they could be said to have social status and economic leeway above the middle class in Joseon society (Shin et al., 2008; Shin et al., 2021).

Figure 1.

The locations of sampling sites (indicated by dots) in West Siberia and South Korea.

The second group that we examined comprised Russian settlers’ crania (n = 73) that had been retrieved from a cemetery next to the settlement at Izyuk, a pioneers’ village built in 1660–1670 on the bank of the Irtysh River (Omsk region, Russia). These settlers had migrated from Eastern Europe and from Northern and Central Russia (Tataurova, 2010; Lee et al., 2019). They were farmers who cultivated wheat, rye, oats, barley, vegetables, and berries (Korona and Tataurova, 2011), and whose diet also included fish from rivers or lakes, and dairy products from domestic or wild animals (Bondarev et al., 2020). This group, currently curated at the Institute of the Problems of Northern Development (Tyumen Oblast, Russia), includes 1297 permanent teeth (Lee et al., 2019).

Anthropological examination of the Joseon-period Korean and West Siberian Russian settlers’ crania was conducted by the same researcher (Lee H.J.). To minimize intra-observer errors, re-examinations were conducted until a definitive conclusion could be reached. Age and sex were estimated using the standard anthropological protocol of Buikstra and Ubelaker (1994). The shape of the symphysis pubis, the auricular surface, ectocranial suture closure, tooth eruption, and dental attrition were used for age estimation. The adolescents’ age was additionally estimated by tooth-formation stages and epiphyseal closure of the long bones. All of the individuals were grouped into four different age categories: 15–19 years, 20–34 years, 35–49 years, and over 50 years (Lee et al., 2019). The teeth were cleaned with a brush for precise examination. We counted LEH cases following the methods of Goodman and Rose (1991) and Buikstra and Ubelaker (1994). Our study used only permanent teeth (not deciduous teeth). Cranial cases with fewer than four teeth were excluded from our study. The rates were calculated in two different ways: per individual and per tooth.

We used R 3.4.0 software (R Foundation for Statistical Computing, Vienna, Austria) for our statistical analysis (R Core Team, 2022). We compared the proportions (homogeneity) of age and sex across the groups by Pearson’s chi-squared test. LEH incidence in each group was statistically tested using the same test. In cases where the total sample number was less than 10, Fisher’s exact test was used for comparison (Lee et al., 2019). We employed the ggplot2 package implemented in R 3.4.0 (Wickham, 2009) to draw a radar chart plotting the data of this report.

Results

As for the issue of homogeneity in the respective age proportions of the Russian settlers and Koreans, we concluded that the age groups were not differently distributed (Fisher’s exact test, P = 0.1388) (Table 1). The sex proportions likewise showed no intergroup difference between the Russian settlers and Koreans (Pearson’s chi-squared test, P = 0.2492) (Table 2). The Russian settlers’ LEH incidence per individual was 4.1% (3/73), while that of the Koreans was 61.5% (56/91) (Table 3). In the case of LEH per tooth, the Russian settlers showed an incidence of 1.9% (24/1297), and the Koreans, 16.8% (336/2001) (Table 4). Thus, the difference in LEH incidence between the two groups was highly significant (per individual: P = 9.188 × 10^–14 for chi-squared test; per tooth: P < 2.2 × 10^–16 for chi-squared test). The detailed data specifying the tooth type are also summarized in Table 5.

Table 1.

Homogeneity in the proportion of age between Russian settlers and Joseon people

Age (years)	Group		P-value between age
	Russian settlers	Joseon people
15–19	8	2	0.1388a
20–34	29	38
35–49	25	37
≥50	11	14

^a Fisher’s exact test.

Table 2.

Homogeneity in the proportion of sex between Russian settlers and Joseon people

		Sex		P-value between sex
		Female	Male
Group	Russian settlers	42	31	0.2492a
	Joseon people	43	48

^a Chi-squared test.

Table 3.

Comparison of LEH prevalence between Russian settlers and Joseon people (per individual)

Age (years)	Russian settlers					Joseon people				P-value
	Total (n)	Affected (n)	Non-affected (n)	Frequency (%)		Total (n)	Affected (n)	Non-affected (n)	Frequency (%)
15–19	8	0	8	0.0		2	2	0	100.0	0.02222*a
20–34	29	2	27	6.9		38	25	13	65.8	3.873 × 10–6***b
35–49	25	1	24	4.0		37	21	16	56.8	6.652 × 10–5***b
≥50	11	0	11	0.0		14	8	6	57.1	0.002929**a
Total	73	3	70	4.1		91	56	35	61.5	9.188 × 10–14***b

^a Fisher’s exact test. ^b Chi-squared test. *P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001

Table 4.

Comparison of LEH prevalence between Russian settlers and Joseon people (per tooth)

Age (years)	Russian settler					Joseon people				P-value
	Total (n)	Affected (n)	Non-affected (n)	Frequency (%)		Total (n)	Affected (n)	Non-affected (n)	Frequency (%)
15–19	113	0	113	0.0		62	26	36	41.9	4.55 × 10–13***b
20–34	620	15	605	2.4		942	185	757	19.6	<2.2 × 10–16***b
35–49	417	9	408	2.2		783	101	682	12.9	1.59 × 10–9***b
≥50	147	0	147	0.0		214	24	190	11.2	6.681 × 10–5***b
Total	1297	24	1273	1.9		2001	336	1665	16.8	<2.2 × 10–16***b

^b Chi-squared test. *P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001

Table 5.

Detailed LEH prevalence by tooth location between Russian settlers and Joseon people

Age	Russian settlers										Joseon people
	Total	I1	I2	C	PM1	PM2	M1	M2	M3		Total	I1	I2	C	PM1	PM2	M1	M2	M3
Adolescent	0	0	0	0	0	0	0	0	0		26	6	6	6	3	2	2	1	0
Young adult	15	4	3	4	2	2	0	0	0		185	31	34	54	28	19	12	6	1
Middle adult	9	3	4	2	0	0	0	0	0		101	23	21	41	11	5	0	0	0
Old adult	0	0	0	0	0	0	0	0	0		24	2	4	11	4	2	1	0	0
Total	24	7	7	6	2	2	0	0	0		336	62	65	112	46	28	15	7	1

Among the Russian settlers, males showed an incidence of 3.2% (1/31), and females, 4.8% (2/42), a difference that was statistically insignificant (Fisher’s exact test, P = 1) (Table 6). In the case of the Koreans, LEH was detected in 68.8% of males (33/48) and 53.5% of females (23/43) (Table 7), a sex difference that was likewise was statistically insignificant (chi-squared: P = 0.2012). The results are summarized in our radar chart (Supplementary Data 1).

Table 6.

Prevalence of LEH by sex in Russian settlers

Age (years)	Male					Female				P-value
	Total (n)	Affected (n)	Non-affected (n)	Frequency (%)		Total (n)	Affected (n)	Non-affected (n)	Frequency (%)
15–19	3	0	3	0.0		5	0	5	0.0	1a
20–34	10	1	9	10.0		19	1	18	5.3	0.3667a
35–49	12	0	12	0.0		13	1	12	7.7	1a
≥50	6	0	6	0.0		5	0	5	0.0	1a
Total	31	1	30	3.2		42	2	40	4.8	1a

^a Fisher’s exact test.

Table 7.

Prevalence of LEH by sex in Joseon people

Age (years)	Male					Female				P-value
	Total (n)	Affected (n)	Non-affected (n)	Frequency (%)		Total (n)	Affected (n)	Non-affected (n)	Frequency (%)
15–19	1	1	0	100.0		1	1	0	100.0	1a
20–34	16	13	3	81.3		22	12	10	54.5	0.1717b
35–49	24	15	9	62.5		13	6	7	46.2	0.5415b
≥50	7	4	3	57.1		7	4	3	57.1	1a
Total	48	33	15	68.8		43	23	20	53.5	0.2012b

^a Fisher’s exact test. ^b Chi-squared test.

Discussion

After the emergence of sedentary agricultural practices, agrarian cultures faced increased risk of disease as well as an overall decline in nutritional intake (Goodman et al., 1980; Cohen and Armelagos, 1984; Latham, 2013). Krenz-Niedbała (2014) reported that mixed subsistence economies (Corded Ware culture) in Polish history had fewer cases of LEH than did agricultural subsistence economies (Lengyel culture). This was likely due to farmers’ excessive reliance on the consumption of a limited range of crops (Cohen and Armelagos, 1984). Generally speaking, farming societies have experienced serious nutritional deficiencies, but also other potentially deleterious syndromes including rapid population growth, poor sanitary conditions, and increased rates of infectious disease. Such deterioration has resulted in much physiological stress among farmers, adversely affecting the health of infants and children (Armelagos and Goodman, 1991; Armelagos et al., 1991).

We should also note that there have been numerous Eurasian societies that lived under quite different circumstances. For example, in 16^th- to 19^th-century Siberia, Russian settlers cultivated wheat, rye, barley, oats, and vegetables, under the cultural influence of the Russian Empire. They were living in Siberia, but maintaining the diet and lifestyle cultivated in European society. Meanwhile, on the eastern side of the Eurasian continent was a long-standing East Asian pattern of agriculture (e.g. Korea and Japan). They had a history of being strongly influenced by the tradition of rice farming over thousands of years. Both of these societies (Russian settlers in Siberia and East Asian rice farmers) on the Eurasian continent had something in common in that they were fundamentally farmers. Yet they also differed in many ways, such as in the crop types cultivated and the lifestyles they lived. The natural environment they live in is also different, affecting the development of their lives differently.

In this sense, the current results show some interesting findings. The Koreans’ LEH rate reached as high as 61.5% per individual, or 16.8% per tooth. Contrastingly, the Russian settlers’ LEH was as low as 4.1% per individual, or 1.9% per tooth (Supplementary Data 1). Since the data were obtained by the same researcher (Lee H.J.), the possibility of observer bias could be ruled out. The far-higher Korean LEH rate would seem to indicate that their physiological stress level during childhood was somehow significantly higher than that of the Russians.

Joseon-period Koreans are not the only historical case of high LEH frequency in East Asia. Japanese scholars have reported rates of LEH per individual in Edo-period Japan (1603–1868 CE) as high as 65.1% (Hitotsubashi) and 61.8% (Wano) (Yamamoto, 1989). Given the similarity of the LEH rate for Edo Japanese to that for our Korean population (61.5%), we presume that such higher LEH rates (above 60%) were common among East Asian societies; and that their LEH ratio prior to the 20^th century was at least much higher than that of Russian settlers who existed further west of the Eurasian continent and maintained a European lifestyle. Therefore, it appears that East Asian societies were more vulnerable to physiological stress than were Russian settlers in Siberia although confirmation remains elusive.

Several hypotheses can be inferred as to the actual cause of such a significant LEH rate difference between Siberia and East Asia. First, we note that the population of Russian settlers were essentially farmers who had moved into Siberia. We presume that they ate high-protein diets comprised of meat, fish, and milk products as staple foods (Bondarev et al., 2020; Tataurova, 2020). Meanwhile, in the 17^th century, East Asian farmers were still cultivating rice in the traditional way as before, and as such, were in a relatively marginalized state during modernization. Certainly, their diets having remained grain-based and low-protein, coupled with what historians believe was a rapid increase in Korean and Japanese populations between the 16^th and 19^th centuries (Kim et al., 2014), might have incurred physiological stress that led, for example, to their much higher incidence of LEH in childhood relative to the Russian Siberians.

The stable isotope data we have already reported are proof of this. Joseon people relied for their subsistence mainly on farming of rice and other grains. According to a previous stable-isotope analysis of Joseon skeletons (Yu et al., 2014), they mostly consumed C3-based foods as the main staples, and the proteins that they ate were mainly of terrestrial origin (only a few were of marine origin). Recently, in a stable-isotope comparison of archaeologically obtained hairs from Russian settlers (n = 13) and Joseon-dynasty people (n = 13), we revealed that the diet of Russian settlers had lower δ¹³C (mean = –21.92‰) and higher δ¹⁵N (mean = 12.16‰) values, compared with the Joseon people (mean = –19.65‰ for δ¹³C; mean = 11.47‰ for δ¹⁵N (Kim et al., 2023)). The stable-isotope data of Kim et al. (2023) revealed that Russian settlers ate more C3 grains and high-protein foods than their Joseon-era Korean near-contemporaries, and that the Joseon people probably consumed more C4 plants but less protein.

However, given the small sample size in this study, our conclusions on physiological stress should be taken with care for now, especially considering that there are additional inducing factors accounting for the prevalence differences of LEH, which were not considered in the present study. In this study, the difference in farming culture and dietary habit might have been one of many possible factors for LEH. However, this reason does not explain all the difference between the two populations. For instance, the natural environment, including the climate between the two regions, may also have been the main cause of the LEH difference between Russian settlers and Joseon people. Rather than forcefully deducing the cause of the difference between the two, it seems appropriate to withhold confirmation of the specific cause, but to simply state that there was a difference for this case.

Finally, we need to discuss the issue of age distribution and sexual dimorphism in LEH. We would like to point out that incidence of LEH shows a significant gap between Russian settlers and Joseon Koreans, but there is not much difference in age proportions as seen in Table 1. This means that LEH indicates stress but it does not affect lifespan and/or average lifespan in both groups of people. We note Amoroso et al.’s proposition that although early life stressors such as LEH seem strongly related to premature mortality, the socioeconomic circumstances of adulthood accounts for most of the decreased longevity (Amoroso et al., 2014).

Next, as for relationship between LEH incidence and sex dimorphism, Tomczyk et al. (2012) speculated that historically much higher LEH incidences in females than in males possibly reflect nutritional-caregiving preferences (e.g. longer breastfeeding duration) for male babies. Other reports, however, present contradictory data: higher LEH rates among males than among females, which could possibly be explained by a generally greater susceptibility of boys to environmental stimuli and stresses (Hoyenga and Hoyenga, 1982; May et al., 1993; Guatelli-Steinberg and Lukacs, 1999; Palubeckaite et al., 2002). In the present study, however, there was no statistical difference in LEH incidence between the sexes in either the Russian-settler or Korean populations. Sexual dimorphism in LEH frequency might not actually be a common phenomenon, at least as concerns the 16^th- to 18^th-century Eurasian continent. Much more data are needed to confirm this hypothesis.

Conclusion

The current report serves to highlight the variability of LEH frequency among different farming societies on the Eurasian continent. Our study of two cranial series of 16^th- to 19^th-century Eurasian farming groups revealed that the LEH incidence of Joseon-period Koreans was far higher than that of Russian settlers in Siberia. It appears that historical LEH frequency on the Eurasian continent was truly diverse, possibly due to divergent and as-yet-unknown stress conditions affecting different groups of people. There have been reports on the LEH incidence of East Asian residents before the 20th century, but the results of simultaneous comparison of how much difference there was from LEH of the residents of other regions are very rare, and in that sense, this study has academic significance.

Acknowledgments

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (no. 2020R1A2C1010708; 2023R1A2C1006785). The present work was also funded by State Task (project no. 121041600045-8 of Tyumen Scientific Center of Siberian Branch) of the Russian Academy of Sciences.

Conflict of Interest

The authors declare that they have no conflicts of interest in this paper.

Author Contributions

Hyejin Lee: conceptualization, data curation, formal analysis, investigation, methodology, writing-original draft, writing-review and editing; Dong Hoon Shin: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, supervision, writing-original draft, writing-review and editing; Larisa Tataurova: investigation, methodology, resources; Jieun Kim: data curation, software, visualization, writing-review and editing; Jong Ha Hong: data curation, funding acquisition, investigation, methodology, writing-review and editing; Sergey Slepchenko: conceptualization, data curation, formal analysis, investigation, project administration, resources, supervision, writing-original draft, writing-review and editing. All authors made final approvals of the manuscript to be submitted.

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