Skeletal evidence for the emergence of i

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 126:359 –376 (2005) Skeletal Evidence for the Emergence of Infectious Disease in Bronze and Iron Age Northern Vietnam Marc F Oxenham,1* Nguyen Kim Thuy,2 and Nguyen Lan Cuong2 School of Archaeology and Anthropology, Australian National University, Canberra, ACT 0200, Australia Institute of Archaeology, Ha Noi, Vietnam KEY WORDS Vietnam; infectious disease; differential diagnosis; health ABSTRACT Human skeletal evidence for the emergence of chronic infectious disease in northern Vietnam is examined The sample includes the remains of 192 individuals representing the Mid-Holocene and Bronze to Iron Ages The objective is to see if the transition from sedentary, foraging, coastally oriented economies to centralized chiefdoms with attendant development and intensification of agriculture, trade, metal technologies, warfare, and population increase was accompanied by an emergence of and/or increase in infectious disease It was found that skeletal evidence for infectious disease was absent in the Mid-Holocene, while over 10% of the Metal period sample exhibited lesions consistent with either infectious disease or immune system disorders Factors potentially contrib- uting to the emergence of infectious disease in northern Vietnam in the Metal period include: increased contact with bacterial or fungal pathogens either directly or by way of vertebrate and/or arthropod vectors; higher levels of debilitation and/or decreased levels of immunocompetence in the Metal period; and evolution of pathogens present in Mid-Holocene human hosts into more virulent forms in the Metal period The first two factors may be related to historically and archaeologically documented major demographic (Han colonizing efforts) and economic (agricultural intensification) changes in the region during the Metal period Am J Phys Anthropol 126:359 –376, 2005 © 2004 Wiley-Liss, Inc This study is concerned with identifying, quantifying, and discussing the implications of skeletal evidence for infectious disease among the inhabitants of the northern portion of the Socialist Republic of Vietnam, during the Mid-Holocene and Metal periods It is based on skeletal remains of 192 individuals excavated from archaeological sites in the region from the 1960s through the 1990s For the most part, previous studies of human skeletal material recovered from Vietnam focused on Late Pleistocene and Holocene morphology, patterns of microevolutionary change, and population movement within East Asia (Demeter, 1999; Demeter et al., 2000; Matsumura et al., 2001; Nguyen KT, 1990, 1998; Nguyen LC, 1985, 1992, 1996; Olivier, 1966; Pietrusewsky, 1988; Pietrusewsky et al., 1992) Oral health (Oxenham and Nguyen, 2002; Oxenham et al., 2002) and the evidence and implications of traumatic injury (Oxenham et al., 2001) in prehistoric northern Vietnamese samples were previously examined However, very little is known regarding the presence, let alone origins and distribution, of skeletally sensitive infectious disease in prehistoric Vietnam For Southeast Asia as a whole, a small and growing body of literature is detailing the presence and distribution of disease in this bioarchaeologically undersampled region of the globe Tayles (1996, 1999) examined the evidence for chronic infectious disease in the form of malaria, and associated biological adaptations to this disease in the form of genetically transmitted hemoglobinopathies, in prehistoric Thailand Indriati (personal communication) analyzed skeletal lesions consistent with tuberculosis in the remains of an individual recovered from a bronze drum inhumation, dated to approximately 2,300 years ago, in central Java, Indonesia Pietrusewsky and Douglas (2002) outlined a range of infections at the 4,100 – 1,800-year-old site Ban Chiang, northern Thailand, including mastoiditis, pulmonary disease, and nonspecific infections identified by way of localized periostitis Tuberculosis may have been present in Thailand in the 5,500 –3,000-year-old assemblage from Non Nok Tha (Pietrusewsky, 1974; Douglas, 1996) and perhaps in the 2,200 –1,700-year-old sample from Noen U-Loke (Tayles and Buckley, in press) Intriguingly, a good argument for the appearance of leprosy at Noen U-Loke has also been developed (Tayles and Buckley, in press) © 2004 WILEY-LISS, INC *Correspondence to: Marc Oxenham, School of Archaeology and Anthropology, Australian National University, Canberra, ACT 0200, Australia E-mail: marc.oxenham@anu.edu.au Received May 2002; accepted February 2004 DOI 10.1002/ajpa.20048 Published online September 2004 in Wiley InterScience (www interscience.wiley.com) 360 M.F OXENHAM ET AL BIOCULTURAL CONTEXT A review of contemporary Vietnam’s climate and geography provides a useful, and for the most part representative, insight into Mid-to-Late Holocene conditions The following summary is drawn from Nguyen TD (1995) Topographically, while about three-quarters of Vietnam can be described as mountainous, 85% of the mountains are below 1,000 m in elevation Vietnam has three plains systems that are still in the process of expansion The archaeological sites of interest here are situated in the northern Bac Bo plain and fall between latitude 18 –22° north This northern plain is low-lying, averaging between 0.3–10 m above sea level Vietnam presents two distinct climatic zones, a northern and a southern Northern Vietnam has two seasons, cold and hot, but with high levels of humidity occurring during both periods The north experiences marked climatic variability or instability that has restricted levels of ecological variation in comparison to the south The area is prone to typhoons, violent storms, and torrential downpours which have caused extensive agricultural and human disruption in the present and the past Coastally, mangroves still predominate, while dense bamboo forests are common all over the northern plains Northern Vietnam is home to a diverse range of bird, riverine, and marine life Some 900 species of fish are recognized in the Gulf of Bac Bo alone Terrestrial animals such as sambar deer, muntjac, chamois, and numerous arboreal primates are still common in the region In the past, elephant, rhinoceros, tiger, and panther were also common The earliest accepted period of anatomically modern human occupation in northern Vietnam, the Son Vi Culture, dates back approximately 30,000 ybp (Nguyen KS, 1996) While the Son Vi continues until some 11,000 ybp, a new culture period, characterized for the most part by lithic artifact morphology, emerged around 18,000 ybp, and is termed the Hoa Binh or Hoabinhian Communities attributable to the Hoabinhian period, which lasts until approximately 6,000 ybp, were involved in hunting and gathering a wide variety of mammals, birds, fish, and shellfish (Higham, 1989), and may have practiced an incipient form of horticulture (Gorman, 1971) The relationship between post-Hoabinhian communities, which are principally coastally oriented, and the Hoabinhian itself is unclear, as the latter is virtually always restricted to inland caves and rock shelters The earliest skeletal material to be examined in this study is sampled from the initial phase of the Da But culture This archaeological culture, lasting for approximately 1,700 years, is considered one of a number of emergent Mid-Holocene cultures with a coastal/marine economic focus that developed out of the Hoabinhian approximately 6,500 ybp (Bui Vinh, 1991, 1994, 1996; Nguyen KS, 1997) Morphologically, these people have been characterized as “Aus- tralo-Melanesians,” in distinction to the Metal period people who are considered “Mongoloid” or Northeast Asian in appearance (Matsumura et al., 2001) Da But sites are for the most part shell middens that include polished stone artifacts, pottery, and arguably domesticated pigs and buffalo as well as human burials (Bui Vinh, 1991) The people are characterized as sedentary foragers with a marked marine/aquatic resource dependency (Yasutomo, unpublished findings) The first appearance of fishing net sinkers, spinning whorls, stone awls, stone chisels, and technological changes in stone axes occur during the Middle Da But, about 5,500 ybp Moreover, there is a large increase in the frequency of polished and curved stone artifacts that have been interpreted as hoes (Bui Vinh, 1991) There is also an increase in the number of domesticated buffalo and pig remains (Bui Vinh, 1996) The final phase of the Da But period, beginning around 5,000 ybp, is characterized by technological changes with respect to pottery and stone artifacts Settlements spread along the coast, and the development of sea travel and sea fishing is suggested (Bui Vinh, 1991, 1996) The next general culture period for which a large sample of skeletal material is available occurs during the development of metal technologies The earliest evidence for metal in northern Vietnam appears in late Phung Nguyen culture contexts, although no skeletal material has been recovered from this period These sites are situated on relatively raised areas to the northern edge of the Red River delta The Phung Nguyen culture, believed to have lasted from 4,000 –3,500 ybp, is notable for its rich and technologically sophisticated array of stone jewelry Following this period, the Dong Dau phase, 3,500 –3,000 ybp, ushers in a major development in bronze-working technology with the appearance of spears and arrowheads, as well as more utilitarian items such as fishing hooks, chisels, and axes The Dong Dau phase is followed by the Go Mun period, 3,000 –2,500 ybp, and is characterized by the development of an enormous range of decorative, utilitarian, ritual, and martial items (Higham, 1996) Emerging from these early bronze phases is the Dong Son culture, flourishing in northern Vietnam from 2,500 ybp until Han domination and colonizing efforts in the first centuries of the first millennium CE Higham (1989, p 30) described the Vietnamese Dong Son as one of several Southeast Asian examples demonstrating social differentiation and a move “from village autonomy towards centralised chiefdoms.” Apart from the diverse range and technological sophistication of material culture objects, e.g., richly decorated bronze drums exceeding 80 kg, there is evidence of marked craft specialization, a complex ritual life, the development of an aristocratic and centralized elite, maritime trade, and sophisticated military skills and equipment One notable example of the material achievements of this 361 INFECTIOUS DISEASE IN BRONZE AGE VIETNAM TABLE Study sample summary Period Sample Abbreviation Region Individuals Date (ybp)1 Da But Dong Dau/Go Mun Go Mun Go Mun Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Total Con Co Ngua Quy Chu Nui Nap Thieu Duong Vinh Quang Min Duc Duong Co Dinh Chang Doi Son Chau Son Dong Xa Quy Chu Nui Nap Nui Nap Dong Mom CCN QC NN TD VQ MD DC DC DS CHS DX QC NN NN DM Ma River Ma River Ma River Ma River Red River Red River Red River Red River Red River Red River Red River Ma River Ma River Ma River Ca River 96 16 13 1 30 192 6,000–5,500 3,300–2,500 3,000–2,500 3,000–2,800 2,200–1,700 2,200–1,700 2,200–1,700 2,200–1,700 2,200–1,700 2,285 Ϯ 452 2,200–1,700 2,450 Ϯ 45, 2,520 Ϯ 552 2,400–2,000 1,670 Ϯ 852 2,200–1,700 Refers to date of skeletal sample Radiocarbon date period can be seen in the surviving earthen structures of the 600 former capital Co Loa, built on the Red River plains some 2,200 ybp The preceding discussion invites the development of a hypothesis that proposes that the populations sampled from both periods will have suffered from infectious disease, but at a higher frequency in the Metal period sample While the population density of Da But period Vietnam is unclear, many midden sites have been identified, and the evidence for reduced mobility is strong for sites such as Con Co Ngua at least An increased degree of residential sedentism and increased population density are also indicated for the Metal period In addition, the subtropical environment and apparent early domestication of large vertebrates suggest the potential for the early emergence of infectious disease either via the environment directly or by way of zoonoses Historical evidence for Han military campaigns and colonization of the region, in addition to intensification of land modification and agriculture in the Dong Song period particularly, increases the probability of the development of infectious diseases at this time In testing this hypothesis, we will examine the evidence for infectious disease in Mid-Holocene and early Metal period Vietnam, and attempt to identify the types of disease that are present in order to better understand the actual health implications Any observed differences in the frequency and nature of infectious disease over time will be discussed within the respective biocultural context of each sample and with respect to current theoretical models of infectious disease MATERIALS AND METHODS Table summarizes the sample sizes, dates, and localities of human remains examined in this study, and Figure shows the location of each site with skeletal remains The Da But period sample is composed of 96 individuals excavated from the MidHolocene site Con Co Ngua in Thanh Hoa Province, northern Vietnam, in 1979 and is dated to between Fig Map of northern Vietnam, showing location of sites with skeletal remains examined in this study (from Oxenham et al., 2002) 6,000 –5,500 ybp (Bui Vinh, 1980) The Metal period sample is an aggregation of 96 individuals from 11 separate archaeological sites in northern Vietnam that spans 3,300 –1,700 ybp The majority of this sample derives from the Dong Son stage, with the remaining individuals belonging to either the Dong Dau or Go Mun phases The level of infracranial preservation in the Da But sample is much better than for the Metal period (Table 2), while both samples display similar levels of cranial and dental preservation The most poorly preserved portions of both samples include the vertebrae, os coxae, and fibulae After the cranium, more robust bones such as the humerus and femur are the best-preserved elements in each assemblage Tropical soils are generally acidic and not conducive to bone preservation Metal period burial practices involved extended burial in soil, whereas at Con Co Ngua, individuals were buried in a squatting pos- 362 M.F OXENHAM ET AL TABLE Major skeletal element preservation Vietnam Da But period Vietnam Metal period Element Expected n Obs1 % Obs Complete Obs2 % complete Expected n Obs1 % Obs Complete Obs2 % complete Cranial Maxilla Mandible Vertebra Sacrum Os coxae Humerus Radius Ulna Femur Tibia Fibula 96 192 96 2,304 96 192 192 192 192 192 192 192 80 126 77 na 23 92 122 103 120 144 115 53 83 66 80 na 24 48 64 54 63 75 60 28 47 58 48 195 21 15 69 49 45 66 43 19 49 30 50 22 36 26 23 34 22 10 96 192 96 2,304 96 192 192 192 192 192 192 192 84 144 74 na 29 44 34 37 43 36 22 88 75 77 na 15 23 18 19 22 19 11 55 86 48 129 18 29 19 21 28 27 15 57 45 50 6 15 10 11 15 14 Includes any state of preservation Includes elements greater than 50% preserved Obs, observed; na, not applicable TABLE Sample sex and age-at-death profiles Vietnam Da But sample Vietnam Metal period sample Age class Males Females Total % Males Females Total % 0–11 months 1–14 years 15–19 years 20–29 years 30–39 years 40–49 years 50ϩ years Indeterminate1 Indeterminate2 Total n % na na 14 11 43 58.1 na na 31 41.9 14 22 14 18 12 96 1.0 6.3 9.4 14.6 22.9 14.6 18.8 12.5 0.0 na na 11 28 44.4 na na 11 35 55.6 11 27 17 13 96 2.1 11.5 9.4 28.1 17.7 9.4 7.3 13.5 1.0 77.1 65.6 Adult but could not be assigned to an age category Too fragmentary to assign as adult or subadult na, not applicable ture within shell midden material The remineralization afforded by this latter practice no doubt contributed to better preservation at Con Co Ngua The age-at-death profiles for each assemblage (Table 3) indicate poor infant and subadult representation The Con Co Ngua sample is skewed toward older ages, with 69% of the sample 30 years of age or older, compared to 48% of the Metal period sample There are also apparent sex imbalances within each assemblage, with a higher ratio of males at Con Co Ngua (1.4:1), and a higher ratio of females in the Metal period sample (1.3:1) Approximately 13% of each sample could not be reliably sexed, and this may account for these differences in assemblage composition Every preserved element of every individual was examined macroscopically for evidence of pathological lesions Where lesions were suspected they were described in detail, photographed, and X-rayed In cases where a systemic condition was suspected, the entire preserved skeleton was X-rayed If observed pathological conditions were characteristic enough to potentially enable identification of the disease process responsible a differential diagnosis was carried out Due to the wealth of descriptive material and sometimes extensive differential diagnoses, these results can only be summarized here RESULTS General health Evidence for general health and well-being in each sample is reviewed here, based on recent work by Oxenham (in press; see also Oxenham et al., 2001; Oxenham and Nguyen, 2002; Oxenham, 2000) These results provide a generalized health context in which to evaluate the evidence and implications for more specific forms of disease in these samples The oral health of the dental sample from Con Co Ngua is good, with low tooth count rates of carious lesions (14/951, 1.5%), abscesses (22/1,430, 1.5%), and antemortem tooth loss (69/1,430, 4.8%) The evidence from cribra orbitalia and enamel hypoplasia suggests somewhat compromised physiological well-being at Con Co Ngua Of all individuals with assessable orbits, 81% (47/58) had lesions on a continuum of active to highly remodeled No statistical significance for the frequency of cribra orbitalia by age-at-death was found The frequency of canine linear enamel hypoplasia by individual (left canine 363 INFECTIOUS DISEASE IN BRONZE AGE VIETNAM TABLE Frequency of nontraumatic lesions Period Bone Lesion type Da But Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Humerus Parietal Frontal Frontal Temporal Os coxae Vertebral body Vertebral articular process Humerus Femur Ulna Lytic Lytic Lytic Blastic Lytic Lytic Lytic Lytic Blastic Blastic Blastic Elements1 Individuals2 n Obs % n Obs % 69 102 54 54 101 18 129 107 29 28 21 1 2 1 1.4 1.0 1.9 3.7 3.0 11.1 1.6 1.9 3.4 3.6 4.8 44 52 54 54 52 12 21 18 20 17 14 1 2 1 2.3 1.9 1.9 3.7 5.8 16.7 9.5 11.1 5.0 5.9 7.1 More than 50% complete Represented by a given element more than 50% complete Obs, observed TABLE Summary of lesion descriptions and differential diagnoses1 Individual2 Sex Age in years Bone Da But 80CCN M74a M 50ϩ Right humerus Dong Son 70DC SA Ϯ 1.5 Period Lesion size (mm) Lesion shape Remodelling Lytic (distal epiphysis) 16.8 Circular S Left parietal Lytic (postero-superior) 7.4 ϫ 5.7 Lesion type/position Oval S, V M1a Differential diagnosis Chondroblastoma Juxta-articular cyst Giant-cell tumor Pigmented villonodularsynovitis Langerhan’s cell histiocytosis Epidermoid cyst Mycotic infection Neolplastic Nonspecific infection Dong Son 89MD F 40–49 Right os coxae Lytic (superior ischial tuberosity) 4.0 Circular V Dong Son M2a 89MD F 20–29 Right frontal Lytic (adjacent to bregma) 7.5 Circular S, V Right frontal Blastic (osteoma on frontal boss) 4.2 Circular S 12.5 ϫ 5.2 Irregular V, P 30.0 ϫ 5.0 9.0 Circular S, V, P 2.0–6.0 Circular Langerhan’s cell histiocytosis Chondroblastoma Aneurysmal cyst Neoplastic Epidermoid cyst Mastoiditis Circular Epidermoid cholesteatoma Sarcoidosis Mycotic infection See 77NN M10ka M7a Dong Son 89MD F 40–49 Left humerus Blastic (periostitis of proximal and mid diaphysis) Dong Son M8a 76NN M 40–49 Left temporal Lytic (suprameatal triangle) M 20–29 Left temporal Lytic (mastoid; multiple) M2c Dong Son 77NN M10Ka Dong Son 78NN Dong Son M7ka 95DX M1a F 30–39 Right temporal Lytic (mastoid; multiple) Langerhan’s cell histiocytosis Epidermoid cyst Neoplastic Mycotic infection Trauma, inflamatory process, neoplasm, genetic Nonspecific localized infection 3.0 F 30–39 Dong Son 84DS F Adult Dong Son M9a 77CHS M 50ϩ Thoracic Thoracic Thoracic Thoracic 10 Left os coxae Left frontal Lytic (articular process) Lytic (articular process) Lytic (body) Lytic (body) Lytic (ischium) Blastic (osteoma on frontal boss) 12.0 16.7 19.0 ϫ 11.5 20.0 na na Circular Circular Oval Circular S Left femur Blastic (periostitis of distal metaphysis) Diffuse Irregular V, P Right ulna Blastic (periostitis of midshaft) 7.5 ϫ 30.0 Irregular V, P M1a Mycotic infection Tuberculosis Osteomyelitis Neoplastic See 89MD M7a Nonspecific localized infection Sex: SA, unsexed subadult; M, male; F, female Remodelling: S, sclerosis observed either macroscopically or radiologically; V, vascular porosity; P, periostitis Number prefixing individual code is excavation year (e.g., 70DC ϭ Duong Co, 1970 excavation); letter/numeral combination on next line represents burial designation (e.g., M1a ϭ burial number 1a) 364 M.F OXENHAM ET AL TABLE Skeletal inventory of individuals with lesions 80CCNM74a Cranial Clavicle Scapula Rib Humerus Radius Ulna Hand Vertebra Sacrum Femur Patella Tibia Fibula Os coxae 70DCM1a Cranial 89MDM2a Cranial Sternum Clavicle Scapula Rib Humerus Radius Ulna Vertebra Os coxae Femur Tibia Fibula Foot 89MDM7a Cranial Humerus Radius Sacrum Femur Tibia Fibula 89MDM8a Cranial Clavicle Scapula Sternum Humerus Radius Ulna Vertebra Femur Patella Tibia Fibula Foot Calva; maxillary arcade from left M1–I1, right arcade from C–M1; mandibular body from P3–M3 and right body from P3–M1 Left complete; right diaphysis Fragment of superior glenoid and coracoid; complete right glenoid and acromion left and right articular fragments, and 18 other small fragments Left complete; right condyles and fragment of proximal head Proximal 1/3 left diaphysis; right nearly complete (missing distal metaphysis) Left proximal 3/4; right head Left M3 proximal 2/3; right M1 and M3 proximal 2/3; proximal row phalanges Dens and left facets of atlas, thoracic centra, L5 centrum Promontory Left distal 3/4; right condyles and proximal 1/3 of diaphysis Left and right complete Left head and distal 1/3; right almost complete Distal articular section of right and section of mid diaphysis Fragment of posterior right ilium and complete auricular area Left side of calva, but includes right orbit and large section of right occipital; maxilla from permanent M1–M1 Fragment of left mandibular body, including unerupted M1 and dm2 alveolus Complete cranium, maxilla, and mandible Complete body Complete left Left and right complete complete left and complete right Complete left Complete right Complete left Complete atlas, T1, T2, T11, T12, L4; complete sacrum (missing coccyx) Left and right complete except for pubic symphyses Complete right Left distal 4/5 Left diaphysis proximal 3/4 Complete left calcaneus Complete cranium; complete maxilla; complete mandible Near complete right Complete right Complete Left proximal 3/4 Left diaphysis proximal 3/4 Left distal 3/4; right complete Complete cranium, maxilla, and mandible Left and right complete Left and right complete Manubrium and sternal body Left and right complete Left and right complete Left and right complete Axis, C3–C7, T2–T11, L1–L5 complete Left and right complete Left and right complete Left and right complete Left and right complete Right talus complete; left and right calcanea complete; left navicular and cuboid; right navicular and cuboid, 1st cuneiform; left and right M2–M5 (continued) or antimere substitution) is 71.7% (38/53), with a mean number of linear events per tooth of 2.4 Again, the frequency of linear enamel hypoplasia by age-at-death was not found to be significant Risks from serious injury are elevated in comparison with other Southeast Asian assemblages For instance, healed fractures (by element) of the femoral diaphysis are 6.5%, and of the humerus, 4.4% The oral health of an aggregated Metal period sample is reasonably good, with no statistically significant differences in comparison to the oral health of the Da But sample in terms of carious lesions by tooth count (26/1,152, 2.3%), abscesses (39/1,518, 2.6%), or antemortem tooth loss (46/1,518, 3.0%) As was the case for the Da But assemblage, the frequencies of cribra orbitalia and enamel hypoplasia suggest compromised physiological health, although there are no significant differences in the frequency of these health markers between temporal periods Of those individuals with assessable orbits, 73.2% (41/56) had active or remodeled lesions No statistical significance for the frequency of cribra orbitalia INFECTIOUS DISEASE IN BRONZE AGE VIETNAM 365 TABLE (continued) 76NNM2c Cranial Clavicle Humerus Radius Ulna Hand Vertebra Femur Patella Os coxae 77NNM10ka Cranial 78NNM7ka Cranial 95DXM1a Cranial Clavicle Sternum Scapula Rib Humerus Radius Ulna Hand Os coxae Vertebra Sacrum Femur Tibia Fibula Foot 84DSM9a Cranial Foot 77CHSM1a Cranial Scapula Humerus Radius Ulna Vertebra Rib Femur Patella Tibia Foot Calva including face; most of maxilla; complete mandible Left medial 1/2; right medial 3/4 Left and right distal 3/4 Left distal 3/4; right proximal 1/4 and mid-diaphysis 1/3 Left proximal and distal 1/3 of diaphysis; right complete Right navicular and capitate, M2 proximal 1/2, M3 distal third; proximal row phalanges, midrow phalanges Left articular facets of atlas, left 1/2 of axis, C5–6 centra Left and right proximal 2/3 diaphysis Left complete Left auricular area including greater sciatic notch, fragment of superior acetabulum; right superior acetabular fragment Much of cranium but missing base; complete mandible Most of maxilla, but right arcade missing posterior to M1 Much of cranium but missing base; complete alveolar process of maxilla; most of mandible, but missing left ascending ramus and condyle Complete cranium, maxilla, and mandible Left diaphysis and acromial end; right complete Manubrium and sternal body Left and right coracoid/acromion/glenoid fossa complexes 23 articular processes preserved, with most including medial 1/3 of shaft; 13 fragments, including central and distal region of the rib Complete left and right Left proximal 2/3; right complete Left proximal 3/4; right complete Left navicular, lunate, capitate, hamate, M1–M5; right lesser and greater multangulars, lunate, hamate, M1–M5; proximal row phalanges, midphalanx, distal row phalanges Left and right complete, except missing pubic symphyses Complete C1–L5 Much of the left lateral portion missing Left and right complete Left and right complete Left and right complete Left and right calcanea and tali complete; left 1st, 2nd, and 3rd cuneiforms, navicular, M1 (distal two-thirds), first proximal and distal phalanges; right first, second, and third cuneiforms, cuboid, navicular, M1 (proximal 1/4), M2–M3, first distal phalanx Calva; mandibular fragment left M3–P3 Left and right tali complete Complete cranium, maxilla, and mandible Right coracoid/acromion/glenoid fossa complex Left complete Left complete Left and right complete Axis, C7–L5 complete complete right Left distal 3/4 Left complete Left complete Left 1st cuneiform by age-at-death was found The frequency of canine linear enamel hypoplasia by individual is 67.3% (37/ 55), with a mean number of linear events per tooth of 2.9 Again, the frequency of linear enamel hypoplasia by age-at-death was not found to be statistically significant Risks from serious injury are very low in comparison with the Da But period and other Southeast Asian assemblages Only one proximal radial fracture (1/14, 7.1%) and one distal ulna fracture (1/14, 7.1%) were noted The apparent high frequencies are due to poor infracranial preservation of the Metal period sample Frequency of nontraumatic lesions Table summarizes the frequency of observed lesions by element and individual for each assem- blage Despite reasonably good preservation of cranial elements at Con Co Ngua, no evidence for cranial lesions was observed Only one nontraumatic lesion was observed in the entire Con Co Ngua infracranial sample with 1.4% of humerii affected, or 2.3% of individuals In the Metal period assemblage, 10.9% (6/55) of those individuals with 50% or more preservation of cranial elements displayed pathological lesions The majority of lesions are lytic, with the temporal bone being the most frequently affected cranial element Only two individuals displayed cranial blastic lesions in the form of button osteomas on the frontal bone The most frequently affected infracranial element is the os coxae, with lytic lesions to the ischial portion in 11.1% of observed elements or 16.7% of individuals One Metal 366 M.F OXENHAM ET AL period individual displayed destructive lesions of the vertebral articular processes and bodies Blastic lesions of the infracranial skeleton presented as localized areas of slight periostitis in the following frequencies: humerus, 3.4% of elements and 5.0% individuals; femur, 3.6% of elements and 5.9% individuals; and ulna, 4.8% elements and 7.1% individuals While it is difficult to estimate the actual overall frequency of lesions for each sample due to the differential preservation of individual skeletons, minimally 10.4% (10/96) of Metal period and 1.0% (1/96) of Da But period individuals displayed nontraumatic pathological lesions Further, while 20% of the Metal period sample covers the earlier Dong Dau and Go Mun periods, only Dong Son period individuals displayed pathological lesions Lesion descriptions Table summarizes the evidence for lesions and the possible disease processes responsible, while Table describes the preservation of each individual displaying a lesion For those cases where the morphology and location or distribution of the lesion(s) invited diagnosis of the underlying disease process responsible, the lesions and individuals are examined here in more detail The first case to be described is the only individual with a nontraumatic lesion from the Da But period sample, a male aged over 50 years His right humerus has a large spherical lesion on the posterior aspect of the lateral epicondyle that has resorbed the posterior face of the condyle and encroached onto the postero-lateral border of the capitulum (Fig 2) The perimeter of the lesion is slightly sclerotic, and the interior walls are smooth with some porosity and discolored with an unidentified black substance There is no sign of vascularity surrounding the lesion, which is 16.8 mm in diameter and 8.0 mm at its deepest A radiographic examination of all the skeletal material attributed to this individual failed to reveal any further lesions The following cases all belong to the Dong Son phase of the Metal period A young child from Duong Co (70DCM1a), represented by cranial remains only, has a lytic lesion on the rear left parietal bone The slightly sclerotic perimeter of this oval lesion is regular and well-demarcated, and it penetrates the outer table and diploe with an average depth of 3.0 mm The floor of the lesion is slightly remodeled or sclerotic A pale but distinct ring of discolored bone encircles the lesion, which is wider inferiorly than superiorly The pale ring of bone is dotted, with numerous tiny pits indicating some degree of vascularity in life (Fig 3) With the exception of the cribra orbitalia, no other pathologies were present, and this was confirmed on X-ray The deciduous maxillary molars, the only preserved primary dentition, were present and did not display any enamel defects A young adult from Minh Duc (89MDM7a) has a circular lytic lesion restricted to the outer table and diploe, with somewhat roughened slightly sclerotic edges and floor, situated just anterior to the coronal suture and just lateral to bregma, high on the right side of the frontal bone (Fig 4) A ring of concentrated pitting completely surrounds the edges of the lesion and averages 2.5 mm in width There is another band of slightly darker, smoother, and shinier bone also surrounding the lesion, which ranges from a minimum width of 5.5 mm to a maximum width of 12.0 mm There is also a small (4.2 mm in diameter) button osteoma on the right frontal tuber There is extensive cribra orbitalia and associated remodeling in both orbits No evidence of oral pathology or enamel defects was observed The Ma River site male 76NNM2c has a large lytic lesion just superior to the external auditory meatus on the left temporal bone (Fig 5) The structures of the external auditory meatus are nearly completely lost postmortem: all that remains is the superior border of the meatus, including most of the temporomandibular joint (TMJ) fossa The lesion is situated directly over the usual position of the suprameatal triangle and is almost perfectly circular, is 9.0 mm in diameter, and intrudes approximately 9.0 mm at its deepest point The floor and the sides of the lesion are roughened, and it is surrounded by scattered porosity with a localized area of periostitis on the posterior border There is no indication macroscopically or radiologically that the lesion communicated with the mastoid antrum Additionally, this individual displayed an extensively remodeled cribra orbitalia Endocranially, there is extensive pacchionian, or arachnoid, pitting running from midfrontal to vertex all along the sagittal plane Very deep meningeal grooves run parallel to the coronal suture with the right one, 15.0 mm in diameter, ending in a large pacchionian lacuna near bregma Numerous pits are present within the left meningeal groove and tributaries The teeth are severely worn, with eight teeth displaying attrition-induced pulp chamber exposure Due to this level of wear, there were numerous alveolar defects of pulpal origin (granulomas/abscesses) A 20 –29-year-old male, 77NNM10ka, from the Metal period site of Nui Nap, presents with extensive destruction of the mastoid process of the left temporal bone Much of the outer table of the mastoid is completely eroded, leaving visible the network of small honeycomb-like sinuses There are several more isolated holes in the superior region of the process just inferior to the most posterior extension of the zygomatic crest, the supramastoid crest There are at least three confluent lesions in this region, ranging in size from 4.5–5.8mm in diameter, with regular smooth sloping edges (Fig 6) There is no sign of pitting or vascularity associated with any of the lesions The latero-posterior aspect of the condyle of the mandible has been eroded There is also the remnant of a circular lesion on the dorso-lateral edge of the condyle The lesion is 2.2 mm in diameter, with smooth edges and walls This may be re- INFECTIOUS DISEASE IN BRONZE AGE VIETNAM 367 Fig 80CCNM74a A 50ϩ year-old male Large lytic lesion on distal epiphysis of right humerus (anterior view) Fig 89MDM7a A 20 –29-year-old female Lytic lesion penetrating outer table and diploe of frontal bone, just forward and to left of bregma (anterior of cranium at right in photo) Fig 70DCM1a Aged years Ϯ 16 months Lytic lesion on posterior aspect of left parietal bone (lambdoid suture at bottom right; dorsal at top of photo) lated to the extensive lytic destruction of the left mastoid Both orbits displayed clear evidence of highly remodeled cribra orbitalia Endocranially, there were pacchionian pits on the left parietal adjacent to the sagittal suture In fact, there is a large (40.0 mm diameter) depression just distal to bregma and bisected by the sagittal suture This is probably a large, shallow pacchionian lacuna This lacuna Fig 76NNM2c A 40 – 49-year-old male Lytic lesion, with associated slight periostitis, situated over suprameatal triangle of left temporal bone (anterior of cranium at left in photo) contains several clusters of smaller pacchionian pits Such extensive granulation activity is unusual in such a young individual (Mann and Murphy, 1990) This individual was free from alveolar defects of pulpal origin and caries, but the maxillary canines and incisors displayed enamel hypoplasia The 368 M.F OXENHAM ET AL Fig 77NNM10ka A 20 –29-year-old male Note well-circumscribed lesions in superior portion of left mastoid and massive destruction of lower aspect of mastoid (anterior of cranium at left in photo) Fig 95DXM1a Note destruction of cortex of T8 (left of photo) and large space-occupying lesions on lateral aspects of T9 and T10 (left lateral view of lower thoracic vertebrae) Fig 95DXM1a A 30 –39-year-old female Note complete destruction of right, inferior interarticular facet of the third cervical vertebra (inferior view) anterior teeth exhibited a deep red betel nut (Areca catechu) stain (Oxenham et al., 2002b) The final individual to be detailed here is the 30 –39-year-old female, 95DXM1a, from the Metal period site Dong Xa The right inferior interarticular facet of the third thoracic vertebra (T3) has been completely destroyed There is extensive porosity surrounding the lesion, or the former site of the articular facet (Fig 7) The corresponding right superior facet of T4 is completely eroded away, with only porous, slightly remodeled trabecular bone re- maining There is extensive erosion of the dorsal and dorso-anterior centrum and the tips of all processes and antemortem erosion of the left superior interarticular facet, which corresponds to slight erosion of the T3 left inferior facet T8 displays erosion of the dorsal, left lateral, and much of the ventral aspect of the centrum A large scooped-out lesion presents in the left lateral aspect of the T9 centrum, which is approximately 12.0 mm in diameter, with a maximum depth of 10.0 mm (Fig 8) The lesion is circular and internally spherical, with the walls and floor being exposed porous trabecular bone There is also considerable erosion of the anterior and antero-ventral aspects of the centrum The left latero-posterior aspect of the T10 centrum presents a large scalloped lesion which extends as far posteriorly as the base of the left lateral transverse process (Fig 8) It is roughly spherical, internally exposing porous trabecular bone, and measures 16.7 mm in diameter by 12.2 mm deep Additional features include erosion of the upper anterior aspect of the centrum and an oval hollow in the antero-dorsal right lateral portion of the centrum The left os coxae has a shallow oval lesion on the medial face of the superior ischial ramus measuring INFECTIOUS DISEASE IN BRONZE AGE VIETNAM 369 ease process represents, in fact, the narrow tails of the normal distribution (Miller et al., 1996, p 225) A nonexhaustive differential diagnosis is presented for those lesions that lend themselves to some specificity in identification of the underlying disease processes involved Diseases inconsistent with the age-at-death or broad geographic location of these Vietnamese individuals are excluded from consideration This search for potential disease culprits will assist in both assessing the human costs potentially associated with the disease load in ancient Vietnam and identifying reasons behind the apparent timing of the emergence of skeletally sensitive diseases in this region of the world Fig 95DXM1a Well-circumscribed, smooth-floored lesion on medial aspect of upper ischial ramus (medial view) 19.0 mm supero-inferiorly and 11.5 mm antero-posteriorly (Fig 9) For the most part it has smooth sloping sides, although there is a sharp border superiorly, due to pressure and fracturing of this region The floor of the lesion is stained a shiny dark brown compared to the adjacent matte yellowish bone There are two distinct shallow pits within the crater of the lesion There is no evidence of porosity or remodeling, and it seems purely lytic in nature There is also a localized and discolored circular area, 14.5 mm in diameter, in the superior region of the iliac fossa There are three small foramina within the discolored area, the limits of which are sharply defined Nonetheless, the surface of the bone appears the same as adjacent bone in texture The discoloration is the same as that found in the floor of the aforementioned ischial lesion The iliacus covers the area where this lesion is located Further, it might also be relevant that the left iliac fossa cradles the terminal extension of the descending colon With the exception of articular changes noted in relation to a healed radial fracture, the only other changes seen were generalized microporosity of most joint surfaces No dental caries were observed, although incisor, canine, and premolar enamel hypoplasia was present Extensively remodeled cribra orbitalia was observed in the left orbit, but was absent in the right Spondylolysis of the fifth lumbar vertebra and a sacral neural arch defect (Oxenham et al., 2001) were also observed A radiographic examination of all skeletal material attributed to this individual failed to detect any further pathologies, and none of the macroscopically identified lesions displayed evidence for sclerosis DISCUSSION Identifying specific diseases An accurate paleopathological diagnosis depends on identification of characteristic bony changes in an expected distribution (“constellation”) This requirement is not met by early cases and by only a minority of fully developed cases Modern material teaches that the “classic” morphologic expression of a given dis- Langerhan’s cell histiocytosis A child aged about years, a young female in her 20s, and a mature male in his 40s displayed cranial lesions consistent with the reticuloendothelial disorder Langerhan’s cell histiocytosis This is a disease of unclear etiology that causes a proliferation, either localized or disseminated, of histiocytes (macrophages) This condition, formerly referred to as histiocytosis X, is subclassified with respect to three forms: localized (eosinophilic granuloma of bone); disseminated acute or subacute (Letterer-Siwe’s disease); and disseminated chronic (multifocal eosinophilic granuloma, or Hand-Schuller-Chritstian disease) (Mazabraud, 1998) The localized form mainly affects older children and young adults, while the disseminated acute form affects children under years of age The skeletal lesions associated with the disseminated chronic form, occurring mainly in later childhood and adolescence, can also be associated with diabetes insipidus and exophthalmos (eyeball protrusion) (Mazabraud, 1998) Ortner and Putschar (1981) pointed out that while the bony lesions in each form are similar, they can be differentiated with respect to distribution The skull is the most commonly affected region, with the localized form (eosinophilic granuloma of bone) commonly presenting as an isolated round or oval defect with a beveled edge The other two forms manifest in the cranium with multiple lytic foci Periosteal reactive bone is not usually seen, even in cases where both tables have been destroyed (Ortner and Putschar, 1981), although a periosteal reaction can occur (Rothschild and Martin, 1993) This form is self-limiting and benign (Ortner and Putschar, 1981), with the lesions able to regress and eventually disappear (Mazabraud, 1998) None of the lesions seen in the Vietnamese material were beveled, and there was clear evidence of increased vascularity surrounding the lesion in each case It is not clear if beveled edges are a crucial diagnostic feature of this condition, and the morphology of a healing or regressing lesion is not clearly described If this condition is responsible for any or all of these lesions, it is the localized eosinophilic granuloma form The lesion affecting the temporal bone in the older male is additionally a good candidate for this form, as 370 M.F OXENHAM ET AL solitary eosinophil granulomas are often localized in the temporal bone (Friedmann, 1974), and the temporal bone is commonly the first affected area in Langerhan’s cell histiocytosis (Brookes and Booth, 1997) Neoplastic disease Included in the differential diagnosis for the aforementioned individuals and a female in her 30s from Dong Xa is some form of neoplastic disease Primary malignant carcinomas are known to metastasize to the cranium, among other sites, and such metastases are by definition malignant (Ortner and Putschar, 1981) In differentiating between malignant and benign lesions, Rothschild and Martin (1993, p 167) suggested that “bone destruction with welldefined margins, easily separated from surrounding normal bone, is generally a sign of a relatively benign process, independent of the smoothness or shagginess of the bone margins.” Under such a definition, the cranial lesions affecting 70DCM1a, 89MDM7a, and 76NNM2c should be regarded as benign, thus excluding them from further consideration as metastases A likely candidate for a benign tumor of the craniofacial region is a chondroblastoma (Mazabraud, 1998) Only considering the temporal lesion of 76NNM2c, it is worth noting that benign cysts frequently form between the angle of the pinna and mastoid region and can readily become infected (Friedmann, 1974) Another possibility is a spread of a tumor or abscess from the pinna to the adjacent temporal region which can occur with basal-cell carcinoma, a nonmetastasizing neoplasm originally of the pinna (Wright, 1997) Aneurysmal cysts, less common than giant-cell tumors but more common than chondroblastomas, should be included when considering 76NNM2c While they are most commonly found in long bone metaphyses, other sites include the skull and especially the temporal bone and mandible (Mazabraud, 1998) The dry-bone morphology of such a cranial focus of this cyst is unclear from the literature The most likely evidence for a chondroblastoma is the epiphyseal lesion in the distal humerus of 80CCNM74a Some 98% of epiphyseal lesions are due to osteomyelitis, chondroblastomas, or giant-cell tumors (Aufderheide and Rodrı´gues-Martı´n, 1998) The lesion under consideration here bears no morphological resemblance to bony changes consistent with osteomyelitis, and this condition can be excluded from further discussion Chondroblastoma is a rare benign tumor accounting for only 1% of all bone tumors (Aufderheide and Rodrı´gues-Martı´n, 1998; Mazabraud, 1998) Apart from their craniofacial distribution, these tumors only form in epiphyseal and apophyseal sites, and some three-fifths of documented modern cases appear in males (Mazabraud, 1998) While some authors suggest that chondroblastomas are more frequently found in younger individuals, with some 70% manifesting in the second decade (Mazabraud, 1998), others argue that the greatest incidence occurs during the third and fourth decades (Resnick and Niwayama, 1981) The most common sites include the humeral and femoral heads, followed by the greater trochanter, cranium, ribs, iliac bones, os calcis, and proximal tibia (Resnick and Niwayama, 1981; Mazabraud, 1998) Other rarer sites include the hands, feet, flat bones in general, and spine (Aufderheide and Rodrı´gues-Martı´n, 1998) None of the aforementioned sources make explicit reference to the frequency of this tumor in the distal humerus Chondroblastomas can range in size from 1–5 cm, have lytic foci, may or may not destroy the outer cortex with expansion, and often display surrounding periostitis (Aufderheide and Rodrı´gues-Martı´n, 1998; Rothschild and Martin, 1993) However, Resnick and Niwayama (1981) suggested that periostitis of the surrounding bone occurs in only about a third of cases They also noted that the lesion is well-defined, and either spheroid or oval and calcification within the lesion can occur about half the time The size, epiphyseal location, well-defined spherical morphology, lack of periosteal reaction, and apparent expansion and subsequent destruction of the outer cortex with respect to the lesion under consideration are consistent with a chondroblastoma The age-at-death of this individual is estimated at 50ϩ years, and while this tumor is most common from the 20s through 40s, it can occur at any age (Mazabraud, 1998) As noted above, this is a benign tumor, probably asymptomatic during the life of the individual, but these tumors have the potential to lead to considerable joint complications (Mazabraud, 1998) The two individuals with button osteomas of the frontal bone are considered here, as the etiology of such bone masses includes a benign neoplasm in addition to mechanical, inflammatory, vascular (Capasso, 1997), and probably even genetic factors (Ruggieri et al., 1998) Finally, a neoplastic etiology for the lytic vertebral lesions seen in 95MXM1a needs to be considered The lower thoracic lesions can be described as having a space-occupying appearance This is a characteristic of both metastatic carcinoma and blastomycosis, but not tuberculosis However, Hershkovitz et al (1998, p 53) noted that in the case of metastatic cancer, the space-occupying appearance is due to “the formation of an expansile bone displacing mass,” with displacing used “as a term to denote bone resorption and reformation at the outer edge of the tumor mass.” This does not describe the appearance of the thoracic lesions in this instance, thus tending to rule out neoplastic disease Epidermoid cyst An epidermoid cyst needs to be considered with regard to the cranial lesions observed in 70DCM1a, 89MDM7a, and 76NNM2c The following discussion of such cysts is based on Mazabraud (1998) The INFECTIOUS DISEASE IN BRONZE AGE VIETNAM epithelial tissue itself can be introduced by way of trauma, and as such, these cysts are commonly found in bones close to the skin and favor the cranium, jaws, and phalanges Radiologically, they are described as forming a clear cavity and can be surrounded by a sclerotic layer Cranially, they can present as well-circumscribed areas of osteolysis that can destroy both tables These cysts can be found at any age and can even develop from an inclusion in the first stages of fetal development Such cysts can disappear suddenly, and continuous growth is said to be rare Mastoiditis Two adults display lytic lesions of the mastoid process consistent with mastoiditis However, the architecture of the mastoid bone can lend itself to pseudopathological diagnoses, as illustrated by Wells (1967) The outer table of the mastoid region is rather thin and easily eroded postmortem, thus revealing numerous air cells Nonetheless, the lesions in the Vietnamese cases appear actual rather than artifactual Extensive bony destruction caused by mastoiditis will no doubt sufficiently weaken the structure of the mastoid to encourage rapid postmortem destruction The combined processes of ante- and postmortem destruction may be difficult to separate in dry specimens If it is accepted that the destruction of this mastoid is in part due to premortem pathology, the most likely candidate is mastoiditis Otitis media (middle-ear infection) is an extremely common condition affecting nearly all children at some stage (Morris, 1998) Such middle-ear inflammatory conditions are categorized with respect to the underlying disease process as well as location in the living individual (Kemink et al., 1993) They can range from an “incidental finding of fluid in the middle ear space to chronic bacterial infection of the mastoid and middle ear cavities” (Morris, 1998, p 26) There is a close association between the high frequency of respiratory disease and high prevalence of middle-ear disease in many Australian Aboriginal communities (Morris, 1998) In reviewing the literature on the etiology of middleear infection, Morris (1998) noted that there is also an apparent but somewhat equivocal link between the frequency of middle-ear disease and socioeconomic conditions Further, some evidence, albeit inconclusive, points to a genetic or racial link to middle-ear disease prevalence Studies of mastoid infection in skeletal remains have focused on population-level radiographic examinations of mastoid air-cell morphology (Gregg and Steel, 1982; Titche et al., 1981) The mastoid’s air cells, which should be well-pneumatized in a healthy individual, are particularly susceptible to pathological alteration during development, in childhood, as a result of ear infection A radiographic examination of 77NNM10ka and 77NNM7ka revealed what appeared to be normal pneumatization, which suggests that the osteolytic lesions were associated with 371 an adult manifestation of the disease Two further conditions that need to be considered are a mycotic infection (discussed below) and sarcoidosis of the ear, both of which can imitate the effects of chronic mastoiditis (Friedmann, 1974) Mycoses A fungal pathogen is potentially implicated in 60% of those Metal period individuals displaying lesions The case is circumstantial for five of these individuals, but strong for the female from Dong Xa Much of the following discussion will focus on 95DXM1a and will include evidence for why several other diseases are improbable The female from Dong Xa presented with lytic lesions to thoracic centra and articular processes as well as the ischium, thus suggesting tuberculosis as a candidate Clinically, the fungal infections blastomycosis (Frean et al., 1993; Guler et al., 1995) and coccidioidomycosis (Wesselius et al., 1977; McGahan et al., 1979) may imitate the signs, including skeletal, of tuberculosis Hershkovitz et al (1998) provided a set of criteria, principally based on lesion morphology, to differentiate between blastomycosis, tuberculosis, and metastatic cancer Although neither blastomycosis nor coccidioidomycosis is endemic to Southeast Asia, the skeletal lesions described for 95DXM1a are consistent with descriptions of the morphology and distribution of lesions seen in these diseases As so few fungal diseases have been described with respect to their specific bony manifestations, it is worthwhile examining the skeletal presentation of these two fungal conditions in more detail as a potential clue to the nature of the condition affecting this individual Hershkovitz et al (1998) described tuberculous lesions of the vertebrae as excavations that may coalesce Blastomycotic lesions, on the other hand, are generally isolated Tuberculosis is a less likely candidate because isolated “tuberculous foci in posterior elements of vertebrae are extremely rare” (Ortner and Putschar, 1981, p 145) On the other hand, vertebral osteomyelitis, which can be difficult to distinguish from vertebral tuberculosis (Sapico and Montgomerie, 1990), will often involve the spinous process and neural arch, although usually only one vertebra is affected, which is not the situation seen in 95DXM1a Finally, actinomycosis needs to be considered in a differential diagnosis when considering tuberculous, blastomycotic, and coccidioidal infections (Crank et al., 1982) Unlike tuberculosis, actinomycosis can affect any part of a vertebra, although centra are preferred sites Crank et al (1982, p 167) noted, however, “[w]hen the thoracic spine is involved the posterior ends of the corresponding ribs also are likely to be affected.” Crank et al (1982, p 167) also described actinomycotic vertebral lesions as presenting “an irregular, saw-tooth appearance,” and reactive new bone is usually present There was no rib involvement in 95DXM1a, and the morphology of the vertebral lesions is not consistent with that caused by actinomycosis 372 M.F OXENHAM ET AL The morphology of the Dong Xa female’s ischial lesion is very different from those of the thoracic vertebrae Hershkovitz et al (1998) described a blastomycotic lesion of a humerus as smooth and elliptical, which is at least consistent with the appearance of the ischial lesion in the Vietnamese case The putative iliac fossa lesion and this ischial lesion are also consistent with a paravertebral or psoas abscess, a condition that occurs in both tuberculosis and vertebral blastomycosis (Saccente et al., 1998) Coccidioidomycosis is a fungal condition that affects the skeleton in some 20% of disseminated cases (Dalinka and Greendyke, 1971) Osteolytic lesions affect most bones, with the axial skeleton being affected in 59% of cases in a recent study (Zeppa et al., 1996) The most common type of lesion has a punched-out or well-demarcated appearance, is more frequently seen in long bones and flat bones, and sometimes has sclerotic margins (McGahan et al., 1979; Zeppa et al., 1996) The presence of more permeative lesions that may affect the vertebral bodies was also described (Zeppa et al., 1996) Osteolytic lesions of the vertebrae can affect the body, pedicles, and transverse processes, and contiguous involvement of the ribs may also occur (Dalinka and Greendyke, 1971) Of a number of fungal infections that potentially involve the bony tissues, histoplasmosis can likely be ruled out, as extensive bony involvement is only seen in the form specific to Africa Sporotrichosis can also likely be eliminated, as vertebral involvement has not been reported (Hershkovitz et al., 1998) Cryptococcosis has a high propensity to affect both the vertebrae and os coxae The specific appearance of cryptococcosis in dry bones is unknown, and it cannot be ruled out at this stage A further fungal condition to consider is penicilliosis marneffei The fungal agent responsible for penicilliosis marneffei, Penicillium marneffei, is a dimorphic fungus endemic to Southeast Asia and southern China (Louthrenoo et al., 1994) Deng and Connor (1985) reported on eight cases from Guang Xi province, southwestern China, discovered between 1964 –1973 The age of affected individuals ranged between 11– 40 years The majority of infected cases were farmers The course of the illness ranged between months and years All cases were described as “disseminated, progressive, and fatal” (Deng and Connor, 1985, p 323) Deng and Connor (1985) pointed out that two species of bamboo rat living in the region could be potential reservoirs of the pathogen, and that these rats are regularly trapped and eaten by local inhabitants There are also Tang dynasty (CE 618 –906) references to the trapping and consumption of rats by the indigenes of the region (Schafer, 1967) Given the extensive liver and intestinal involvement in their five autopsied cases, Deng and Connor (1985) suggested that ingestion of the pathogen by way of eating infected rats is a likely cause of human infection However, in a later paper, Deng et al (1986) argued that it is unlikely that the bamboo rat is instrumental in human infection by the fungus, and surmised that an as yet unknown environmental factor is responsible for both rat and human infection While Deng and Connor (1985) noted bone marrow involvement in all their autopsied cases, no mention was specifically made of osteolytic lesions However, in a study of five cases reported from Thailand, two individuals displayed osteolytic lesions (Yayanetra et al., 1984) In one case, a male aged 35 years, lesions to the proximal femur, greater trochanter, clavicle, scapula, sternum, ribs, and big toe were described In the other case, a female aged 50 years, a lesion on the right frontal bone was described More recently, Louthrenoo et al (1994) examined eight individuals from Thailand manifesting penicilliosis marneffei They describe the osteolytic response thus: The osteomyelitis manifested as multiple osteolytic lesions with minimal sclerotic margin involving flat bones, long bones and small bones of the hands and feet There was no periosteal reaction One patient (case 2) who had cervical spine involvement had an osteolytic lesion at the posterior portion of the axis (Louthrenoo et al., 1994, p 1148) Louthrenoo et al (1994) went on to suggest that the distribution of osteolytic lesions seen in these instances of penicilliosis marneffei has been reported for other mycotic infections, and as such they are not unique to this particular condition The morphology and distribution of lesions seen in 95DXM1a would appear to be consistent with some form of mycotic infection A mycotic infection also needs to be considered with respect to the lesions seen in the child from Duong Co and the young female from Dong Mom Further, a fungal pathogen may have been responsible for the mastoid destruction seen in 77NNM10ka and 78NNm7ka Yagi et al (1998, p 68) stated that mycetoma (Madura skull in this instance) “should be considered in the differential diagnosis of mastoid bone pathology in the tropics.” They reported on a 22-year-old Sudanese female, with mycetoma of the mastoid, which resulted in bony destruction of the mastoid, and they suggested that the fungus was probably introduced into the ear by way of an ear-cleaning implement Typically, the pathogen is introduced via traumatic inoculation Implications of the frequency and nature of infectious disease For most of the 20th century the prevailing dogma held that disease organisms should eventually evolve toward benign coexistence with their hosts This traditional view point is flawed because it fails to cast the problem in the context of natural selection (Ewald, 2003, p 117) Clearly the evidence indicates a much greater level of skeletally sensitive infectious disease in the Metal period of Vietnam, and this occurs despite the comparatively much poorer level of infracranial preservation of this sample It might also be argued INFECTIOUS DISEASE IN BRONZE AGE VIETNAM that the osteological evidence for infectious disease first appears in the Metal period of this region The following discussion will examine the implications of these findings in the context of the types of diseases arguably identified, evolutionary models of pathogen behavior, the immunocompentence of the samples, and the social, behavioral, and demographic changes occurring during the Metal period Without recourse to modeling the natural history of pathogens and hosts within the context of evolutionary theory, the appearance of infectious lesions in Metal period Vietnam could be interpreted as an accommodation between formerly highly virulent pathogens and human hosts For instance, Ortner (1991, p 11) suggested that “[t]he evolutionary tendency for infectious agents to become less virulent with time will increase the probability that older diseases will be more chronic in their relationship to the host.” However, it has become clear that pathogens will tend to evolve toward higher virulence, particularly when the pathogens involved are either water-borne or vector-borne (Ewald, 1994, 2003) One possible scenario is the emergence of pathogens new to human hosts in the Mid-Holocene with the adoption of more sedentary lifeways and early animal domestication Over time, these pathogens evolved into more virulent forms that had a negative impact on the health of Metal period communities Alternatively, this evolutionary model need not be invoked to account for the situation in northern Vietnam The differential diagnoses indicate the possibility of mycotic diseases in more than 60% of those cases where some level of diagnostic specificity was possible Given the ecology and behavior of the fungal pathogens implicated here, the mode of transmission into human hosts was probably casual or accidental, with no means for transmission of the pathogen directly between human hosts Pathogens that not target humans as hosts can be extremely virulent when they infect humans Examples include Rocky Mountain spotted fever, caused by the transmission of Rickettsia rickettsii through ticks and rabies caused by bat lyssaviruses In northern Vietnam there is equivocal evidence that the Vietnamese bamboo rat plays an important role in the epidemiology of at least one mycotic infection Higher population density and/or altered living conditions and lifeways, particularly land clearing and the development of extensive drainage and irrigation systems in the Red River delta (Holmgren, 1980) in the Metal period, may have led to increased human exposure to such disease-carrying vectors and fungal pathogens directly The level of general health and immunocompetence is also relevant when discussing opportunistic mycoses with a predilection for debilitated or immunosuppressed hosts, such as penicilliosis marneffei If general measures of physiological health in the form of enamel hypoplasia and cribra orbitalia are considered some gauge of the level of sample immunocompetence, it would seem that both the Metal and Da But period 373 assemblages had less than optimal immune systems The lower proportion of older individuals in the Metal period sample is also relevant in this context Further evidence for compromised immune systems in the Metal period is the possible presence of Langerhan’s cell histiocytosis Compromised immunocompetence associated with changes in the way in which humans were interacting within their environment in the Metal period may have led to an increase in mycoses, or a range of other infectious diseases for that matter Tuberculosis was included in the differential diagnosis of the young female from Dong Xa The appearance and frequency of tuberculosis are closely associated with both increased levels of crowding, poor levels of nutrition, and lowered immunocompetence The earliest historical references to tuberculosis in China place it at 4,700 ybp, although clear descriptions of symptoms not appear until 2,400 ybp (Johnston, 1993) However, one confounding factor, not mentioned in such historical research, is that fungal infections (e.g., blastomycosis) may imitate the signs of tuberculosis (Guler et al., 1995; Frean et al., 1993) It is possible that mycoses, rather than tuberculosis, are being described in early Chinese historical accounts Clearly there is no simple relationship between the sample frequency of lesions per se and the level of population health An assemblage with individuals displaying lesions consistent with chronic tuberculosis may be defined as healthy in consideration of their management of the pathogen over time An equally valid inference is that the sample is clearly in a state of poor health, based on the inability of individuals to rid themselves of the pathogen Health is a highly relative and consequently fluid construction, and must be assessed within the context of the type of diseases affecting any given sample However, isolating a specific disease is not straightforward and may never be a practicable aim in many instances This inability to definitively isolate specific pathogens responsible for the lesions seen in the Metal period makes it extremely difficult to infer the relative health of the sample The question of relative health aside, other factors potentially contributory to the apparent emergence of infectious disease in the Metal period need to be examined Numerous studies presented evidence supporting a positive association between increases in the frequency of infectious disease and changes in settlement patterns and/or subsistence economy This correlation was reported for Eastern Europe (Angel, 1984); South Asia (Kennedy, 1984); Japan (Suzuki, 1991); Australia (Webb, 1995); North America (Cassidy, 1984; Cook, 1984; Goodman et al., 1984; Larsen, 1984; Perzigian et al., 1984; Rose et al., 1984; Eisenberg, 1991; Milner, 1991); Central America (Norr, 1984); and South America (Ubelaker, 1994, 2003) Interestingly, a review of research carried out in Western Europe failed to find an unequivocal increase in infectious disease from the Mesolithic to Neolithic periods (Meiklejohn et al., 1984; Meiklejohn and Zvelebil, 1991) However, 374 M.F OXENHAM ET AL part of the explanation for this may lie in the observation that trends toward increased population density were already evident in Western European Mesolithic samples (Meiklejohn and Zvelebil, 1991) A study of preagricultural and agricultural samples from Southwest Asia found a decrease in observed infectious disease frequency over time (Rathbun, 1984) However, it was proposed that the adoption of agriculture resulted in an increase in acute disease that is not represented in the skeletal samples analyzed (Rathbun, 1984) A number of researchers highlighted the link between changing settlement patterns, adoption of sedentism, and increased population density, rather than the adoption or intensification of agriculture per se, and the increase in infectious disease prevalence (Allison, 1984; Armelagos, 1990; Cook, 1984; Larsen, 1984, 1995) It was also demonstrated that contact between hitherto separate cultures can have dire health consequences (e.g., Larsen and Milner, 1994) Increases in the frequency of chronic infectious disease, over and above historically documented marked increases in acute infectious disease, were reported in postcontact North America (Stodder, 1994) and South America (Ubelaker, 1994) Moreover, clear evidence for a decline in postcontact Mayan health, but without evidence for chronic infectious disease, was interpreted as being due to the weeding-out effects of high mortality from acute infection (Cohen et al., 1994) Furthermore, Suzuki (1991) suggested that the first appearance and subsequent high frequency of chronic nonspecific infection and specific infectious disease, such as tuberculosis, in post-Jomon Japan can be attributed to more than subsistence changes and increasing population density alone Perhaps more importantly, this increase in infectious disease can be understood in the context of major human migrations into Japan from the Korean peninsula during the third to seventh centuries CE (Suzuki, 1991) This is potentially a significant factor with respect to the Vietnamese situation during the Metal period The Han had a major social and demographic impact on northern Vietnam during and subsequent to the early Metal period (Holmgren, 1980; De Crespigny, 1990) The massive scale of the demographic changes can be seen in census figures from the period The CE census for the Han prefectures, encompassing the Metal period samples examined in this study, identified 92,440 households in Jiao Zhi and 35,743 households in Jiu Zhen The figures for CE 140 showed an eightfold population increase for Jiao Zhi to 739,520, while in Jiu Zhen the population increased four- or fivefold to 164,418 (Holmgren, 1980) Coupled with these major demographic changes were concerted Han efforts to develop and intensify agricultural production with the aim of “feeding the new immigrant population and supplying coastal shipping, rather than supporting indigent native populations” (Holmgren, 1980, p 5) Not only were the Vietnamese required to make major subsistence changes; they may not have had access to the fruits of their labor Importantly, these demographic and economic changes occurred during the Dong Son culture phase, which is the only sampled phase of the Metal period to show skeletal evidence of infectious disease For the most part, the original hypothesis is supported in that a greater frequency of infectious disease in the Metal period sample is expected In summary, it appears that the Metal period sample, in stark contrast to the temporally earlier Da But period assemblage, displays the skeletal manifestations of infectious disease The possible implications of this include the following 1) There was increased contact with bacterial and/or fungal pathogens directly (e.g., air- and water-borne spores) or indirectly by way of vectors (e.g., rodents and arthropods) in the Metal period This could have been facilitated by changes to the environment-hostpathogen dynamic Two probable examples include increasing population density and land clearing/cultivation Alternatively, or in addition, migration and colonizing efforts by the Han Chinese may have contributed to the introduction and/or spread of infectious disease 2) There were elevated levels of debilitation and/or decreased levels of immunocompetence in the Metal period This may have been caused by changes in the diet with the intensification of agriculture, increased pathogen loads brought about by increased population density and declining levels of sanitation, or relatively recent relocation into the region and consequently less locally adapted immune systems 3) There was an emergence of infectious disease in the sedentary foraging communities of the Da But period and subsequent evolution into more virulent forms A synergy among various combinations of these factors also needs to be considered ACKNOWLEDGMENTS The authors are indebted to and thank a number of individuals for assistance in this project: Ha Van Tan, Director of the Institute of Archaeology, Hanoi, for access to the skeletal material used in this study; and Michele Toomay Douglas, Dave Weaver, and Heather Gerhart for comments on 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