Elsevier

Tuberculosis

Volume 125, December 2020, 101995
Tuberculosis

Oldest evidence of tuberculosis in Argentina: A multidisciplinary investigation in an adult male skeleton from Saujil, Tinogasta, Catamarca (905–1030 CE)

https://doi.org/10.1016/j.tube.2020.101995Get rights and content

Highlights

  • The oldest case of tuberculosis infection in Argentina is described, dated 905–1030 CE.

  • Multiple lesions compatible with tuberculosis were identified in vertebrae, ribs and long bones.

  • Mycobacterium tuberculosis complex lipid biomarkers and aDNA data confirm the presence of the disease.

  • The disease probably arrived in Fiambalá valley from Northern Chile and dispersed towards the northeast to the Yocavil valley.

Abstract

The Mycobacterium tuberculosis complex (MTC) has affected South American populations since ca. 200 years BCE. In Argentina, possible cases date from ca. 1000–1400 Common Era (CE). This paper describes the oldest (905–1030 CE) confirmed case of tuberculosis (TB) in a young adult male from Lomitas de Saujil (Tinogasta, Catamarca, Argentina). Osteolytic lesions on the bodies of the lower spine were macroscopically and radiographically identified. Bilateral new bone formation was seen on the visceral vertebral third of several ribs and in long bones, compatible with hypertrophic osteoarthropathy. Representative rib and hand bones gave profiles for MTC-specific C27–C32 mycocerosic acid lipid biomarkers; these were strongest in one heavily-lesioned lower rib, which also had MTC-diagnostic C76–C89 mycolic acids and positive amplification of MTC-typical IS6110 aDNA fragments. During the first millennium CE, the intense social interaction, the spatial circumscription of villages among the pre-Hispanic societies in the mesothermal valleys of Catamarca and the fluid contacts with the Eastern lowlands, valleys and puna, were factors likely to favor disease transmission. It is proposed that TB arrived from northern Chile and dispersed towards the northeast into the Yocavil valley, where several cases of TB infection were macroscopically identified for a later chronology.

Introduction

Tuberculosis is an infectious disease that has affected humans since at least 10,000 years ago [[1], [2], [3], [4], [5], [6]]. From a bioarchaeological perspective, the identification of tuberculosis in ancient skeletons can provide insights about the type of lesions produced, characteristics of the host and pathogen genomes, dissemination routes, host species, coinfection situations, and associations with other skeletal indicators of stress [3,4,7,8]. It can also contribute to a better understanding of the epidemiological processes of contagion and development of the disease in current human populations. In addition to the study of paleopathology, aDNA analyzes during the last three decades have revealed a greater knowledge of the presence of the disease, its dispersal around the globe and the identification of the Mycobacterium spp. involved [9,10]. Retrieval of full genomes provides comprehensive data on the infecting Mycobacterium species [11,12]. An alternative biomarker approach is the analysis of characteristic mycobacterial cell wall lipids [9,13]. Good examples that complement aDNA amplification were obtained from ancient bison [14] and the oldest human TB cases from the Eastern Mediterranean [1,3]. Commonly used lipid types are the C70–C90 mycolic acids and C27–C34 mycolipenic and mycocerosic acids, as reviewed by Minnikin et al. [13], Lee et al. [15] and Donoghue et al. [9].

The Mycobacterium tuberculosis complex (MTC) has affected human populations in South America at least from ca. 200 Before Common Era (BCE) [[16], [17], [18]]. Most of the pre-Columbian confirmed cases, both skeletons and mummies, are located in the coastal desert of Peru and Northern Chile, where contextual variables favoring the transmission of the infection, such as sedentarization, overcrowding, malnutrition, lack of household ventilation and hygienic deterioration, began about 2000–2500 years ago [10,16,19].

The first report of ancient tuberculosis in South America was of a mummy of a young adult male from Cuzco (Peru), dated ca. 1400–1500 CE, with thoracic vertebral destruction and fusion [20]. Lung histology revealed fibrous tissues that may have had a tuberculous origin. Subsequently, Requena [21] published a case of probable tuberculosis in a pre-Columbian mummy from Venezuela. The first confirmed evidence was based on pathological, radiological and bacteriological methods in a mummified child from Nasca, Peru, dated ca. 700 years CE [22]. Later, mycobacteria were confirmed in several mummies (ca. 200 BCE-1600 CE) from central-southern Peru and northern Chile [16]. Buikstra and Williams [23] studied 37 individuals (ca. 1350 CE) with tuberculosis from Estuquiña (Southern Peru) and conducted the first paleoepidemiological research on this topic. Salo et al. [24] and Arriaza et al. [25] reported the first DNA confirmations of human tuberculosis using PCR techniques, in mummies from Peru (1000–1300 CE) and Chile (ca. 1040 CE). Some years later, Romero Arateco [26] described detailed macroscopic and radiologic research on a guane mummy from Santander, Colombia. Lombardi and García Cáceres [27] identified pleuro-pulmonary and osseous tuberculosis in an adult Nasca male (ca. 900 CE) based on macroscopic, radiological, molecular, and paleoepidemiological diagnoses. More recently, Klaus et al. [28] identified five skeletal cases from the late pre-Hispanic and Colonial-era Lambayeque Valley Complex, northern coastal Peru (900–1750 CE), integrating macroscopic information, radiographs and CT scan images, with DNA analysis. Guichon et al. [29] presented macroscopic lesions from a young male (dated ca. 1300 CE), probably consistent with tuberculosis, with preliminary molecular results from Myren (Southern Chile). Finally, Toyne et al. (2020) evaluated the presence of tuberculosis in the northeastern highlands of Peru (800–1535 CE) through the macroscopical analysis of osseous lesions from Pre-Contact Kuelap, Chachapoyas. Using a population-based approach, the authors stated that skeletal evidence was highly consistent with tuberculosis in 13 individuals, with variations in lesion distribution, which is important to identify the diversity in extra-vertebral tuberculosis lesions.

In Argentina, pre-Hispanic evidences of tuberculosis are based on paleopathology and very scarce. García Guraieb [30] described osteolytic lesions in vertebral bodies of the lower column of a female skeleton (ca. 1200 CE) from a group of hunter-gatherers who lived in the Salitroso Lake basin (Santa Cruz province, Southern Patagonia). The author claims that the osteological analysis allows hypothesizing a probable case of TB infection, although the social context related to low population density makes this case doubtful. More consistent paleopathological macroscopic evidence of pre-Hispanic tuberculosis was found in the burial site Rincón Chico 21 (1300–1500 CE) located in the Yocavil valley (Catamarca, Northwestern Argentina) [31]. The authors reported six individuals with destructive lesions in the vertebral bodies and proliferative periosteal reactions in several bones, interpreted as being caused by mycobacterial infections.

Although tuberculosis in pre-Columbian populations has been clearly recognized in South America, there are few confirmed cases using molecular and chemical analyses [32], and only initial knowledge of the vectors and routes of contagion and dissemination were hypothesized. This paper describes the lesions on a male individual using multiple analytical methods (macroscopic, radiographic, molecular and chemical). It is clear that tuberculosis was present in Argentina towards the end of the first millennium CE, at the time of the development of village societies in Western Tinogasta. This individual is the most ancient case known in Argentinian territory to date and contributes to our understanding of the routes of dispersion of this disease in the Southern Andes during pre-Hispanic times.

Section snippets

Archeological site

The valley of Fiambalá (Catamarca province, Northwest Argentina) was inhabited throughout the first millennium CE by agropastoral societies with a village life. Between 1000 and 1250 CE the region was depopulated because of environmental instabilities. After ca. 1250 CE, when the environmental conditions improved, it was repopulated during the Inca conquest as groups of people were mobilized in the process of domination strategies [33]. Systematic bioarchaeological investigations have been

Macroscopic analysis

The skeleton belonged to a young adult male with an age-at-death about 25–35 years. The individual under analysis is very complete, which allowed the observation of almost all the skeleton. Both the pelvis and the skull suggest a male. Age-at-death was more difficult to estimate. Definitely, he was an adult, because all the epiphyses are fused. The auricular surface and the pubic symphysis points to a young adult. In the maxillae there is little alveolar retraction, low incidence of caries (n

Discussion

The male individual exhumed from the site Lomitas de Saujil is well preserved. The age at-death estimations from the coxae as well as oral health conditions points to a young adult (aged about 25–35 years old) and are consistent with those recorded for other young adults recovered from the region, but the degenerative lesions on his right knee suggest an older age. Knee osteoarthritis has a multifactorial etiology but it is usually a degenerative disease of the cartilage affecting elderly

Conclusions

A multi-methodological investigation was applied to an adult male with macroscopic and radiographic lesions compatible with tuberculosis. This diagnosis was confirmed by the identification of cell wall mycolic and mycocerosic acids and aDNA of the M. tuberculosis complex. Based on these findings, this evidence can be considered highly consistent or typical of tuberculosis. This pre-Inca individual represents, so far as is known, the oldest known case of tuberculosis in Argentine territory and

Declaration of competing interest

None.

Acknowledgements

To Imagen Test facilities for the radiographs. To Dominic Alcock and Michael Li who separately examined the samples for the presence of IS6110 and IS1081; these studies were carried out at the Centre for Clinical Microbiology, Royal Free Campus, University College London, Roland Hill Street, London NW3 2 PF. To three anonymous reviewers who improved the content of this paper through their comments and suggestions. This research was supported by the Agencia Nacional de Promoción Científica y

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