Brief communication New evidence of tuberculosis from prehistoric KoreaЧPopulation movement and early evidence of tuberculosis in far East Asia.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 136:357–360 (2008) 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 1 Department of Epidemiology, Tokyo Metropolitan Institute of Gerontology, Tokyo 173-0015, Japan Department of Anthropology, Niigata College of Nursing, Niigata 943-0147, Japan 3 Kyongnam Archeology Institute, Shinjyu 660-911, Korea 2 KEY WORDS tuberculosis; Bronze Age; population history; Korea; paleopathology ABSTRACT 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. THE NUKDO 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 V WILEY-LISS, INC. C MATERIALS 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. E-mail: firstname.lastname@example.org Received 10 September 2007; accepted 20 December 2007 DOI 10.1002/ajpa.20811 Published online 5 March 2008 in Wiley InterScience (www.interscience.wiley.com). 358 T. SUZUKI ET AL. 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 www.interscience.wiley.com.] 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 www.interscience.wiley.com.] 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 www.interscience.wiley.com.] 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 NEW EVIDENCE OF TUBERCULOSIS IN KOREA 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. wiley.com.] 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 kyphosis. 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 359 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. wiley.com.] probably derived from direct extension of either infected vertebrae or pulmonary abscesses in contact with the overlying ribs. DIFFERENTIAL DIAGNOSIS 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 360 T. SUZUKI ET AL. 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. DISCUSSION 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. ACKNOWLEDGMENTS 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. LITERATURE CITED Canci A, Minozzi S, Tarli S. 1996. New evidence of tuberculous spordylitis from Neolithic Liguria (Italy). Int J Osteoarch 6:497–501. 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). 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