2017 Volume 125 Issue 1 Pages 9-14
In paleoparasitology, which is the study of ancient parasite species, parasite egg remnants in archaeological samples are examined by microscopic or molecular analysis. The parasitological information thus obtained can inform speculation about the parasite-infection patterns that prevailed in ancient societies. The current analysis of ancient feces removed from Joseon period mummies adds six new paleoparasitological outcomes to the existing pool of mummy parasitism data already maintained in South Korea. The current microscopic examination revealed the ancient parasite eggs of Trichuris, Clonorchis, Paragonimus, Ascaris, and Taenia in the Joseon mummy feces. When the updated Joseon data were compared with the 20th-century National Survey statistics of South Korea, clear differences could be observed between ancient and modern parasite infection rates. These results will yield invaluable insights—unobtainable by conventional historical investigation—that contribute to the knowledge base on the parasitism of pre-industrial East Asian societies.
We as paleoparasitologists have partially reconstructed a number of pre-industrial Korean parasite-infection prevalences by scientific techniques. Specifically, by analyzing ancient parasite eggs remnant in archaeological samples, we have managed to reveal the patterns of infection and their changes over time.
Among the samples used for this purpose, the ancient feces discovered in Joseon dynasty (1392–1910 CE) mummies have proved the best, simply because their preservation status tends to be far in advance of those of any other parasitological samples obtained in Korea. Over the past decade, they have become an indispensible resource for studies seeking to understand historical parasite-infection patterns.
Briefly, in our previous studies on the ancient feces, we have employed microscopic or molecular techniques to discover different kinds of ancient parasite eggs such as Ascaris, Trichuris, Clonorchis, Paragonimus, Metagonimus, Gymnophalloides, Strongyloides, Enterobius, Taenia, and Trichostrongylus (Seo et al., 2007, 2008, 2010, 2014a, b; Shin et al., 2009a, b, 2011, 2012a, b, 2013a, b, 2014, 2015; Oh et al., 2010a, b, 2015; Kim et al., 2014). From a series of studies on Korean mummy feces, we constructed the existing corpus on Joseon mummy parasitism (n = 18). We revealed that the overall positive ratios for Ascaris and Trichuris in Joseon mummies were 50.0% and 77.8%, respectively. Although the infection prevalence of the ancient parasitism is only based upon crude estimations, these have been very helpful both in answering queries and raising new questions about historical Korean parasite-infection patterns (Seo et al., 2014a).
Notwithstanding this wealth of significant parasitological data, paleopathologists endeavoring to draw meaningful conclusions on the health and disease statuses of ancient peoples are still hampered by a lack of information. Efforts, for example, to find and confirm any differences in parasitism between pre-industrial and modern Korean people must await paleoparasitological reports based on additional cases representing a variety of geographical and temporal strata.
We report herewith additional parasitological data derived from newly discovered Joseon mummies dating from the 16th–18th centuries. By consideration of the current findings in conjunction with previous reports from other Joseon cases (Seo et al., 2014a), we can make conjectures with regard to the patterns of parasitism prevailing among pre-industrial East Asian people and changes to these patterns caused by modernization.
In this study, we examined ancient feces (n = 6) collected from the intestines of Korean mummies (Hwasung, Andong, YG2-4, YG2-6, Dalsung, Junggye mummies) found in Joseon tombs (Figure 1). Figure 2 shows the place where each mummy was discovered. The archaeological information is summarized in Table 1.
One of the Korean mummies (Hwasung) examined in this study.
Map of South Korea. Red dots mark the archaeological sites where the Korean mummies investigated in this study were discovered. 1, Hwasung; 2, Andong; 3, YG; 4, Dalsung; 5, Junggye.
| Cases | Estimated date in history | Estimated age (years) | Sex | Social position by cultural remains | Other diseases identified |
|---|---|---|---|---|---|
| Hwasung | 18C | 41.3a | M | Rich middle-class people (jungin) based on cultural remains. | No diseases |
| Andong | 16C | 45.4a | M | A minor official (chambong); economically poor yangban (gentry) | Diaphragmatic hernia |
| YG2-4 | 15C–16C | >60b | F | Housewife from a family of official or at least of upper-middle class. | No diseases |
| YG2-6 | 15C–16C | 50–59b | F | Similar to YG2-4. | Schmorl’s node (LV1, 2); compression fracture (LV1) |
| Dalsung | 16C–17C | ND | F | Housewife from upper-class family (yangban). | No diseases |
| Junggye | 16C–17C | 25–29b | M | A man of Han clan. His socioeconomic status looks high based upon the cultural remains from the tomb, | No diseases |
Ancient feces from the intestines (colon) were collected during dissection of the mummies. Each specimen (1–4 g) was rehydrated in 0.5% trisodium phosphate solution while shaking continuously (van Cleave and Ross, 1947; Pike, 1968; Han et al., 2003; Reinhard and Urban, 2003). They were then filtered through multiple-layered gauze and precipitated for a day. The precipitates were dissolved once again in 0.5% trisodium phosphate solution (final volume: 20 ml). The solution was dropped onto slides for light microscopy examination (BH-2; Olympus, Tokyo, Japan). A total of 200 μl of each sample was examined: 20 μl each time, 10 times. The sizes of the parasite eggs were measured. The current data were added to the existing corpus on Joseon mummy parasitism accumulated to date (Seo et al., 2014a). The sizes of the parasite eggs were measured, and the numbers of eggs per gram (EPG) were estimated. They were also compared further with the national survey statistics for 1971, 1981, 1992, 2004, and 2012 (Korea Association of Health Promotion, 2012).
Microscopic examination of the mummy feces revealed the following variety of ancient parasite eggs: Trichuris and Clonorchis in Andong; Trichuris, Paragonimus, and Ascaris in Hwasung; Trichuris, Paragonimus, and Ascaris at YG2-4; Trichuris, Paragonimus, and Ascaris at YG2-6; Trichuris and Ascaris in Dalsung; Trichuris, Ascaris, and Taenia in Junggye (Figure 3). The data on average egg size and EPG are summarized in Table 2. Supplementary Data 1 shows the current findings added to the existing corpus on Joseon mummy parasitism already maintained (Seo et al., 2014a), therefore finally representing a total number of 24 cases.
The ancient parasite eggs discovered in each mummy feces. From top to bottom rows, Andong, Hwasung, YG2-4, YG2-6, Dalsung and Junggye. Scale bars, 30 μm.
| Mummy case | Parasite eggs discovered | Egg size | Eggs per gram |
|---|---|---|---|
| (Length) × (Width) (μm) | |||
| Andong | Trichuris | (55.0 ± 0.0) × (28.3 ± 2.9) | 7737.2 |
| Clonorchis | (30.3 ± 1.0) × (15.7 ± 0.6) | 4744.5 | |
| YG2-4 | Trichuris | (50.3 ± 2.3) × (25.5 ± 0.5) | 838.7 |
| Paragonimus | (85.0 ± 5.4) × (51.3 ± 2.4) | 7516.1 | |
| Ascaris | (60.0 ± 5.9) × (49.6 ± 1.8) | 4096.8 | |
| YG2-6 | Trichuris | (51.3 ± 1.3) × (25.6 ± 1.1) | 183.7 |
| Paragonimus | (85.0 ± 2.5) × (53.0 ± 1.0) | 10.2 | |
| Ascaris | (74.2 ± 10.3) × (55.6 ± 1.4) | 10.2 | |
| Dalsung | Trichuris | (51.3 ± 1.3) × (25.0 ± 0.0) | 761.6 |
| Ascaris | (69.2 ± 4.2) × (50.0 ± 2.0) | 3332.0 | |
| Hwasung | Trichuris | (50.0 ± 0.0) × (25.0 ± 0.0) | 74.6 |
| Paragonimus | (83.3 ± 7.2) × (53.3 ± 2.9) | 74.6 | |
| Ascaris | (65.0 ± 0.0) × (50.0 ± 0.0) | 74.6 | |
| Junggye | Trichuris | (51.2 ± 2.7) × (26.7 ± 1.2) | 80.0 |
| Ascaris | (71.3 ± 9.8) × (48.8 ± 1.3) | 480.0 | |
| Taenia | (32.5 ± 0.0) × (32.5 ± 0.0) | 80.0 |
We compared this Joseon data with the National Survey statistics for 1971, 1981, 1992, 2004, and 2012 (Table 3). For soil-transmitted helminths, the crude infection prevalences in the Joseon period were 58.3% for Ascaris (14/24) and 83.3% for Trichuris (20/24), respectively. Although the National Survey rates for 1971 (Ascaris: 54.9%; Trichuris: 65.4%; total helminth egg-positive rate: 84.3%) were lower than the Joseon rates (Korea Association of Health Promotion, 2012), the differences were not significant. From 1971, however, the South Korean Ascaris- and Trichuris-infection prevalence dropped dramatically, an abrupt change possibly induced by the country’s rapid industrialization. By 2012, the egg-positive rates for Ascaris and Trichuris had fallen to only 0.03% and 0.41%, respectively, while the total helminth egg-positive rate was as low as 2.6% (Table 3).
| Survey of (%) | ||||||
|---|---|---|---|---|---|---|
| Joseon samplesa | 1971b | 1981b | 1992b | 2004b | 2012b | |
| Ascaris | 58.3 | 54.9 | 13.0 | 0.3 | 0.05 | 0.03 |
| Trichuris | 83.3 | 65.4 | 23.4 | 0.2 | 0.27 | 0.41 |
| Clonorchis | 25 | 4.6 | 2.6 | 2.2 | 2.4 | 1.9 |
| Paragonimus | 33.3 | 0.09 | 0 | 0.0 | 0.002 | 0.0 |
| Total egg positive rate | 100 | 84.3 | 41.1 | 3.8 | 3.7 | 2.6 |
We next compared the currently updated crude infection prevalence of trematode species Clonorchis and Paragonimus during the Joseon period with the 20th century National Survey statistics (Table 3). Whereas the liver fluke Clonorchis had infected as many as 25% (6/24) of the Joseon individuals examined, the infection prevalence in 1971 was found to be only 4.6%. The crude infection prevalence for the lung fluke Paragonimus among Joseon mummies—as high as 33.3% (8/24)—also attracted our interest, as by 1971, only 0.09% of South Korean people showed positivity (Korea Association of Health Promotion, 2012).
We admit the limitations of this study from a statistical perspective. Above all, the number of Korean mummies used for the current examinations is not sufficient for deducing authentic conclusions. In addition, the mummified people in this study do not represent the entire Joseon population because they were of higher social status. It is also important not to consider the Joseon period as static, as great changes occurred in Joseon people’s health and disease status over the 500 years. Even so, as there has been very little historical information on parasitism in Korea, our paleoparasitological reports using ancient feces from Joseon mummies have academic value in themselves; and should not be ignored completely.
Over the past several years in South Korea, several paleoparasitological reports on mummies discovered in 15th- to 18th-century Joseon tombs have appeared. Among the ancient parasite eggs identified have been Ascaris, Trichuris, Metagonimus, Paragonimus, and Clonorchis, all detected during microscopic examinations (Seo et al., 2014a). Additional reports providing supplementary information to the existing Joseon data pool, however, remain essential to the soundness and reliability of paleoparasitologists’ speculations and conclusions on the state of ancient parasitism and rates of infection.
Our current reconstruction of Joseon parasitism, we believe, is very important to the paleopathological history of Korea. In fact, whereas the parasite-infection rates of Joseon peoples were generally higher than those of their 20th-century descendants, the patterns of decrease over time differ for each parasite species (Seo et al., 2014b). Briefly, from Joseon times until 1971, the trematode-infection rates dropped sharply from 25% to 4.6% and from 33.3% to 0.09% for Clonorchis and Paragonimus, respectively. Contrastingly, in the case of soil-transmitted parasites, the infection rates were not so remarkably different; significant decreases were observed, rather, in the later 20th century, specifically between the 1971 and 1992 surveys (from 54.9% to 0.3% for Ascaris; from 65.4% to 0.2% for Trichuris).
We were unable to determine why the rates of soil-transmitted parasitism fell much later than did those of trematode infection (Seo et al., 2014b). Clues to the understanding of this phenomenon probably are to be found, for example, in the practice of East Asian farmers in the 17th–18th centuries of recycling night soil as fertilizer for maintenance of farmlands. In the course of fertilizer preparation and utilization, human feces contaminated by Ascaris or Trichuris eggs could readily have been transmitted to vegetables. Consumption of contaminated vegetables would then have initiated a vicious cycle of soil-transmitted parasitism whereby people repeatedly reinfected themselves (Kim et al., 2014).
Indeed, it seems likely that as long as farmers continued to use night soil for their fertilizer, the rates of parasitic reinfection would not have reduced much at all in East Asian countries. Only once chemical fertilizers replaced night soil could Ascaris and Trichuris infection be significantly reduced (Kim et al., 2014). This would explain why soil-transmitted parasitism in South Korea dropped so dramatically from the 1970s, when, not coincidentally, rapid industrialization was making chemical fertilizer available in large quantities to farmers.
In the present study, ancient feces removed from Korean mummies of the Joseon dynasty were analyzed, yielding results that add new data to the existing paleoparasitology corpus. The paleoparasitological data, especially in comparison with 20th-century National Survey data, can provide insights into ancient parasitism in Korea that would not be obtainable by any other forms of conventional research. According to this report, from Joseon to the modern period, the overall rates of parasitism changed dramatically, showing unique decreasing patterns in soil-transmitted and trematode parasitism. This reconstruction of ancient Korean parasitism, furthermore, will be accelerated by forthcoming studies on archaeological samples collected from sites representing a much wider variety of geographic and temporal strata.
This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2013R1A1A2009688).
| Ancient parasite eggs | ||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Mummy case | Estimated date | Ascaris lumbricoides | Trichuris trichiura | Hookworm | Enterobius vermicularis | Clonorchis sinensis | Paragonimus westermani | Metagonimus yokogawai | Gymnophalloides seoi | Strongyloides stercoralis | Trichostrongylus spp. | Taenia |
| (1) Yongin | 15C–16C | ○ | ○ | ○ | ||||||||
| (2) Jinju | 15C–16C | ○ | ○ | ○ | ||||||||
| (3) Sapgyo | 16C | ○ | ○ | ○ | ○ | |||||||
| (4) Hadong-2 | 16C–17C | ○ | ||||||||||
| (5) Hadong-1 | 17C | ○ | ○ | ○ | ||||||||
| (6) Sacheon | 17C | ○ | ||||||||||
| (7) Gangneung | 17C | ○ | ||||||||||
| (8) Dangjin | 17C | ○ | ○ | ○ | ||||||||
| (9) Mungyeong | 17C | ○ | ○ | |||||||||
| (10) Waegwan | 17C | ○ | ○ | |||||||||
| (11) PJ SM | 17C | ○ | ○ | |||||||||
| (12) Seocheon | 17C | ○ | ○ | |||||||||
| (13) Yangju | 17C | ○ | ○ | ○ | ||||||||
| (14) SN1-2 | 17C–18C | ○ | ||||||||||
| (15) SN3-7-1 | 16C–17C | ○ | ||||||||||
| (16) SN2-19-1 | 18C | ○ | ○ | |||||||||
| (17) SN2-19-2 | 18C | ○ | ○ | |||||||||
| (18) GJ1-2 | 17C–18C | ○ | ○ | ○ | ○ | ○ | ○ | |||||
| (19) Hwasung | 18C | ○ | ○ | ○ | ||||||||
| (20) Andong | 16C | ○ | ○ | |||||||||
| (21) YG2-4 | 15C–16C | ○ | ○ | ○ | ||||||||
| (22) YG2-6 | 15C–16C | ○ | ○ | ○ | ||||||||
| (23) Dalsung | 16C–17C | ○ | ○ | |||||||||
| (24) Junggye | 16C–17C | ○ | ○ | ○ | ||||||||
Mummy parasitism results of (1)–(18) represent the existing corpus on Joseon mummy parasitism (Seo et al., 2014a). The current results are (19)–(24).
