вход по аккаунту


Brief communication New evidence of tuberculosis from prehistoric KoreaЧPopulation movement and early evidence of tuberculosis in far East Asia.

код для вставкиСкачать
Brief Communication: New Evidence of Tuberculosis
From Prehistoric Korea—Population Movement and
Early Evidence of Tuberculosis in Far East Asia
Takao Suzuki,1* Hisashi Fujita,2 and Jong Gyu Choi3
Department of Epidemiology, Tokyo Metropolitan Institute of Gerontology, Tokyo 173-0015, Japan
Department of Anthropology, Niigata College of Nursing, Niigata 943-0147, Japan
Kyongnam Archeology Institute, Shinjyu 660-911, Korea
tuberculosis; Bronze Age; population history; Korea; paleopathology
Tuberculosis has been recognized in
Japan and Korea for more than 500 years in historical
medical documents. However, the origin and early existence of tuberculosis is poorly understood in these regions.
Very recently, skeletal evidence for tuberculosis from the
Bronze Age (or Aneolithic) period was reported from
Japan and Korea. This article describes a possible case of
spinal tuberculosis from an archeological site in Korea,
which was dated to the first century BC. This date corresponds to the Aneolithic (Yayoi) period in Japan. Skeletal
evidence for tuberculosis during the Bronze Age period
found in both Korea and Japan are, therefore, discussed
as evidence of the earliest tuberculosis outbreaks in East
Asia and as biological indicators of population movement
between Korea and Japan during this period. Am J Phys
Anthropol 136:357–360, 2008. V 2008 Wiley-Liss, Inc.
The history of tuberculosis has been well studied. In
East Asia, early outbreaks of tuberculosis were related
to migrations of people from the 5th century BC to the
3rd century AD. During this period, there were largescale migrations from Korea to the Japanese Archipelago
via the Sea of Japan. In China, iron weapons and infantry arms were first deployed during the ‘‘Spring and
Autumn period’’ (770–476 BC) and ‘‘Warring States
period’’ (475–221 BC). In 108 BC the Han Dynasty
conquered the northern peninsula and established three
military commandaries in the region. During this commandary period (108 BC–AD 313), the southern peninsula developed Korean nondecorated pottery culture and
acquired new iron and stoneware technologies. Further,
in Japan, Jomon culture characterized by magnificent
cord-marking (‘‘Jomon’’) pottery was mostly replaced by
Yayoi culture, characterized by less flamboyant ceramics,
knowledge of bronze and iron technologies, and systematic development of wet-field rice agriculture. These new
technologies were introduced by many waves of migrants
from the Korean peninsula.
So far, at least three cases of tuberculosis from China
and Japan have been found and dated to this same temporal sequence. However, evidence of tuberculosis has
not been reported from prehistoric Korea.
In this article, the authors describe the earliest case of
spinal tuberculosis from the Bronze Age in Korea. This
case represents the earliest evidence of spinal tuberculosis
in Korea and also helps clarify current knowledge regarding the spread of tuberculosis from China to Japan.
2006). Together with the ‘‘Nukdo’’ pottery, a large number of ‘‘Sugu I’’ and ‘‘Sugu II’’ potteries imported from
Kyushu, Japan, were found at the Nukdo site. These
potteries are representative of the middle Yayoi period
dating from 100 BC to 0 AD. Besides these potteries,
Chinese coins from Shu were also recovered at the
Nukdo site. These archeological materials, particularly
the variation in pottery styles, suggest that this small
island was a trade center between the southern part of
Korea and the northern part of Kyushu.
The skeletal remains of more than 200 individuals
were unearthed during various excavations between
1985 and 1999. Adult remains were found in pit graves,
while the remains of infants and children were found in
earthenware coffins. Antemortem tooth ablation was confirmed among adults. Besides human skeletal remains,
dogs were recovered from the burials at Nukdo. Numerous pieces of animal bones including the scapulae of
cattle showing characteristic cracks by burning, which
acted as a traditional method of prognostication in ancient China, Korea, and Japan, were also found at this
archeological site.
Nukdo island is located off the coast of Sachon in the
southern part of Korea (see Fig. 1). The Nukdo archeological site produced a large amount of non-decorated
pottery (‘‘Mumon pottery’’) which is classified as ‘‘Nukdo’’
Mumon pottery (Kyongnam Archeological Institute,
C 2008
Skeleton no. 117 was found lying on its back, left side
down, perhaps coffined, with some fragments of the
*Correspondence to: Takao Suzuki, M.D., Ph.D., Department of
Epidemiology, Tokyo Metropolitan Institute of Gerontology, 35-2
Sakae-cho, Itabashi-ku, Tokyo 173-0015, Japan.
Received 10 September 2007; accepted 20 December 2007
DOI 10.1002/ajpa.20811
Published online 5 March 2008 in Wiley InterScience
Fig. 2. Left lateral view showing collapse and wedge-shaped
Th-12 fusing with Th-11. Vertebral body of L-1 also showed
severe destruction. [Color figure can be viewed in the online
issue, which is available at]
Fig. 1. Map of the Nukdo archeological site and skeleton no.
117 lying on its back with left side down at the time of excavation. [Color figure can be viewed in the online issue, which is
available at]
Nukdo type pottery which dated from 100 BC to 0 AD
(see Fig. 1). More than 90% of the individual skeleton
was recovered; bones lost to postmortem processes
included the scapulae, most the pelvis and sacrum, the
vertebrae L-2 to L-5, and most of the phalanges.
Morphological features of the cranium and postcranial
skeleton indicated that the individual was female. Dental attrition, epiphyseal union, and pubic symphysis
morphology suggested an age of 15–20 years.
After cleaning and reconstruction of the fragmented
spine, the first to fourth thoracic vertebrae were mostly
complete. The 5th to 10th thoracic vertebrae had partial
defects in the vertebral bodies and spinal processes. Particularly the vertebral bodies from Th-7 to Th-10 were
lost by postmortem damage. The 11th and 12th thoracic
vertebrae were fused. These two last thoracic and the
first lumbar vertebral bodies had collapsed ventrally during life in association with severe pathological changes.
The whole surface of vertebral body Th-11 showed considerable erosion due to inflammatory reactions. Multiple small and larger confluent cavities were localized on
the anterior part of the body. The inner trabeculae were
thickened and partially dissolved indicating haematogeneous spread of the infection via the anterior longitudinal ligament. Intervertebral joints of Th-11 and Th-12
were completely fused probably because of unusually
heavy strain following the destruction of the body of Th12 (see Fig. 2).
The central part of the body of Th-12 was completely
obliterated by severe osseous destruction. The exposed
trabecular bone that constituted the lateral pillars of the
American Journal of Physical Anthropology
Fig. 3. The central part of the bodies of Th-11 (upper) and
12 (lower) from the anterior aspect showing remarkable destructive and resorptive changes, with exposed trabecular bone.
[Color figure can be viewed in the online issue, which is available at]
remaining spongy bone showed active resorptive and
destructive changes. Both sides of its latero-superior
border were fused to the inferior plate of Th-11. The
remaining part of Th-12 consisted of the posterior segment of the vertebra including both sides of the pedicules and laminae, parts of intervertebral joints and the
spinous process (see Fig. 3).
At the 1st lumber vertebra, almost half of the body
had disappeared in association with the osteolytic process. The collapsed body resulted in a wedge-shape
appearance in L-1. The anterior part of the remaining
body was most affected by the disease. The whole surface of the body was eroded with destructive and resorptive changes. Multiple small and larger confluent cavities were also characteristically localized on the central
and lateral aspects of the body, and were recognized as
severe inflammatory processes (see Fig. 4).
Destructive processes on the vertebral body suggested
either a bilateral or circumferential paravertebral abscess. The surface of the remaining body also had resorptive changes resulting in exposure of the inner spongy
Fig. 4. Anterior aspect of the vertebrae from Th-11 to L-1
(a), and a close-up view of the vertebral body of L-1 (b) showing
multiple small and larger confluent cavities with severe destruction due to inflammatory processes. [Color figure can be viewed
in the online issue, which is available at www.interscience.]
structure. There was a large cavity in the antero-inferior
part of the body, suggesting a relationship between these
vertebral cavitations and abscesses. Massive resorption
and collapse of the vertebral body of Th-12 resulted in
marked kyphosis of the thoraco-lumbar vertebral column.
The antero-posterior axis of the corresponding vertebrae
was bent forward at 608. Consequently the spinous process of Th-11 became the salient point of the angular
The marked pathological features from the 11th thoracic to the 1st lumber vertebrae with angulated gibbus
formation due to collapse of the 12th thoracic vertebra
could certainly be considered as characteristic changes of
spinal tuberculosis. Furthermore, the coexistence of
severe resorptive and partial new bone formation in this
individual most likely indicates the active phase of an
infectious process. Radiographic examination of the vertebrae confirmed the findings of macroscopic observation.
Lateral radiographs revealed a mixture of circumferential resorptive lesions and marked radiodense images
corresponding to reactive lesions.
In addition, extensive periosteal plaques were found
on the visceral surfaces of the lower left ribs (probably,
9th to 12th). Some reactive bone was broken away postmortem revealing the underlying cortex, which had minimal changes (see Fig. 5). The periosteal plaques covered
areas from 2 to 5 cm in length. These lesions were
Fig. 5. Anterior aspect of a middle left rib (a), and a closeup view (b) showing periostitis with coarse and proliferative
changes on the visceral surface of the rib. [Color figure can be
viewed in the online issue, which is available at www.interscience.]
probably derived from direct extension of either infected
vertebrae or pulmonary abscesses in contact with the
overlying ribs.
Differential diagnosis of skeletal tuberculosis in paleopathology relies upon destructive and reactive vertebral
and rib lesions as well as collapse and kyphosis (Roberts
and Buikstra, 2003). However, the following pathological
conditions should be considered in the differential diagnosis (1) nonspecific pyogenic inflammation as a result of
severe trauma or destructive spinal osteomyelitis; (2)
brucellosis; and (3) fungal infections including blastomycosis. Among the conditions that may lead to collapsed
vertebrae, destruction of several adjacent vertebrae,
spine angulation, and paravertebral abscesses, nonspecific pyogenic inflammation may be relatively common
while the other two conditions are rare in East Asia as
already discussed by the authors (Suzuki and Inoue,
2007). Nonspecific inflammation or destructive spinal osteomyelitis is difficult to differentiate from tuberculosis
of the spine. However, massive destruction of several
vertebral bodies in osteomyelitis uncommonly leads to
sharply angulated gibbus (Ortner and Putschar, 1981).
Rib involvement is common in tuberculosis (Roberts
et al., 1994). Proliferative lesions on the visceral surface
of ribs accompanied by resorptive lesions on the thoracic
American Journal of Physical Anthropology
and lumbar bodies observed in the present case are more
consistent with tuberculosis.
Since human Mycobacterium bovis infection is indistinguishable from M. tuberculosis infection even in modern man with respect to pathogenesis, lesions, and clinical findings (Moda et al., 1996), it is not possible to specify which species of Mycobacterium was responsible for
the case of tuberculosis presented in this study.
The earliest evidence of tuberculosis in Europe comes
from a grave near Heidelberg, Germany dated to 5000
BC, and also in Italy dated to 3500–4000 BC (Formicola
et al., 1987; Canci et al., 1996). In the far East, the earliest case of tuberculosis with angular deformity of the
spine was reported from the late Longshan period
(4500–4000 BP) in China (Pechenkina et al., 2007).
Another possible case of tuberculosis from China was
described in a female cadaver from the Western Han
Dynasty dated to 200 BC (Hunan Medical Institute,
1980). The oldest cases of tuberculosis discovered so far
in Japan were two cases with both spinal and rib lesions
dated between 454 BC and AD 124, which strongly suggest that tuberculosis first appeared in Japan during the
Aneolithic ‘‘Yayoi’’ period, probably transmitted by immigrants from the Korean peninsula to Japan (Suzuki,
1991; Suzuki and Inoue, 2007).
In evaluating the early occurrence and transmission of
tuberculosis in the far East Asian region during the
Bronze Age, the following two factors should be considered: First, population movement to escape the chaos of
wars during the Spring and Autumn and the Warring
States periods in China likely transmitted tuberculosis
to Korea. During these periods, migration to safer
regions or forced evacuations brought scores of people
into the Korean territory. The continuous movement of
people from the northern to southern part of the Korean
peninsula would have greatly influenced migration to
the Japanese Archipelago across the Japan Sea.
Another important factor influencing the early outbreak and transmission of tuberculosis in this region is
rice agriculture. Rice and the art of its cultivation
reached Japan both directly from regions south of the
Yangtze River in China and from Korea between the 5th
and 2nd century BC (Yasuda, 2002). Cultural changes
from the Jomon to Yayoi period accompanying the development of agriculture led to the development of sedentism, urbanism, and human crowding, all of which are
linked to infectious diseases such as tuberculosis.
From a microevolutionary point of view, the early
occurrence of tuberculosis, and the coexistence of both
Korean and Japanese style potteries indicate that the
Nukdo site was a center of trade and cultural exchange
between southern Korea and northern Kyushu during
the Bronze Age. Various infectious diseases including
tuberculosis and probably measles and small pox were
also exchanged and transmitted between these two
American Journal of Physical Anthropology
regions. In this context, the two reported spinal cases
found in Japan together with the case found in Korea
provide evidence of population movements or migrations
during this period in this region.
This research was supported by the Japanese Ministry
of Education, Sports and Culutre (Grant-in-Aid for Scientific Research in 2004–2006). The authors are indebted
to Dr. Daniel Temple of the Department of Anthropology,
The Ohio State University for his review of this manuscript.
Canci A, Minozzi S, Tarli S. 1996. New evidence of tuberculous
spordylitis from Neolithic Liguria (Italy). Int J Osteoarch
Formicola V, Milanesi Q, Scarshini C. 1987. Evidence of spinal
tuberculosis at the beginning of the fourth millennium BC
from Arene Candide Cave (Liguria. Italy). Am J Phys Anthrop
Hunan Medical Institute. 1980. Study of an ancient cadaver in
Mawangtui Tomb No. 1 of the Han Dynasty in Changsha. Beijin: Editorial Board of the Study of an Ancient Cadaver in
Mawangtui Tomb No. 1. (In Chinese with English summary).
Kyongnam Archeological Institute. 2006. Nukdo Shellmound (V)
Archaeology. Shinju: Kyongnam Archeological Institute. (In
Moda G, Daborn CJ, Grange JM, Cosivi O. 1996. Zoonoic importance of M. bovis. Tubercl Lung Dis 77:103–108.
Ortner DJ, Putschar WGJ. 1981. Identification of pathological
condition in human skeletal remains. Washington DC: Smithsonian Institution Press.
Pechenkina EA, Benfer RA Jr, Ma X. 2007. Diet and health in
the Neolithic of the Wei and Middle Yellow River Basins,
Northern China. In: Cohen MN, Crane-Kramer GNM, editors.
Ancient health: skeletal indicators of agricultural and economic intensification. Gainesville: University of Florida Press.
p 255–272.
Roberts CA, Buikstra JE. 2003. The bioarchaeology of tuberculosis. A global view on a reemerging disease. Gainesville:
University of Florida Press.
Roberts CA, Lucy D, Manchester K. 1994. Inflammatory lesions
of ribs: an analysis of the Terry collection. Am J Phys Anthropol 85:169–182.
Suzuki T. 1991. Paleopathological study on infectious disease in
Japan. In: Ortner DJ, Aufderheide AC, editors. Human paleopathology: current syntheses and future options. Washington
DC: Smithsonian Institution Press. p 128–139.
Suzuki T, Inoue T. 2007. Earliest evidence of spinal tuberculosis
from the aneolithic Yayoi period in Japan. Int J Osteoarcheol
Yasuda Y. 2002. Origin of pottery and agriculture in East Asia.
In: Yasuda Y, editor. The origins of pottery and agriculture.
Yangtze River Civilization Programme. Singapore: Lustre Press.
p 119–142.
Без категории
Размер файла
358 Кб
tuberculosis, koreaчpopulation, prehistoric, evidence, movement, brief, communication, east, far, new, early, asia
Пожаловаться на содержимое документа