THE ANATOMICAL RECORD 298:1111–1115 (2015)

Short Review: Magnetic Resonance Imaging of Ancient Mummies € FRANK J. RUHLI* Swiss Mummy Project, Centre for Evolutionary Medicine, Institute of Anatomy, University of Zurich, Winterthurerstr. 190, Z€ urich 8057, Switzerland

ABSTRACT Noninvasive imaging of ancient tissues is of increasing interest in palaeopathological studies, with conventional X-ray and computed tomography currently considered the diagnostic gold standard. Convenitional X-ray has a long tradition, yet imaging of ancient mummies using conventional X-ray technique has its drawbacks too. Until recently, magnetic resonance imaging (MRI) of soft tissues was successful with ancient dry tissues only after morphology-altering rehydration. This process was deemed necessary due to the previous reported lack of unbound protons. Hitherto, any approach without rehydration of the historic samples failed. Yet, the successful application of novel MRI techniques allows broadening of the methodological spectrum of methods for noninvasive studies on ancient corpses, whether they have wet or dry soft tissue, or bone. Spatial discrimination of chemical elements can now be carried out with high sensitivity in any historic specimen, leading to an increased level C 2015 Wiley of diagnostic evidence. Anat Rec, 298:1111–1115, 2015. V Periodicals, Inc.

Key words: radiology; computed tomography; mummy; paleopathology; soft tissue

PREVIOUS USE OF MAGNETIC RESONANCE IMAGING To achieve an improved differentiation of historic mummified tissue, new methods based on magnetic resonance imaging (MRI)1 have recently been applied in the field of palaeoradiology. Magnetic resonance tomography makes use of the object’s own physical characteristics, detecting tissue-specific reactions to the influence of very potent magnetic fields—currently clinical system run, for example, on 1.5 Tesla (T) in field strength—and radio waves by means of images or deep profiles. The usual lack of moisture in historical material, however, makes such an examination exceedingly difficult. Hitherto, MRI of historic skeletal or mummified remains has not been very successful. Clinical magnetic resonance imaging of soft tissues was hitherto successfully applied in ancient dry tissues only after invasive morphology-alterating rehydra-

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An MRI terminology glossary can be found on the Website of the American College of Radiology at www.acr.org (assessed 1st of April 2010).

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tion (Piepenbrink et al., 1986; Sebes et al., 1991), a process deemed necessary due to the anticipated lack of unbound protons. Any approach without rehydration of the historic samples failed previously (Lewin, 1983; Lewin and Notman, 1983; Notman, 1983, 1986; Notman et al., 1986a,1986b; Drenkhan and Germer, 1991; Hunt and Hopper, 1996; Appelboom and Struyven, 1999; R€ uhli and B€oni, 1999). Leading textbooks in the field specifically mention the failure of MRI to be feasible in desiccated mummy research (Cockburn et al., 1998; Aufderheide, 2003; David, 2008). Only frozen or wet

Grant sponsor: M€ axi foundation Zurich; Grant sponsor: Forschungskredit, University of Zurich. *Correspondence to: F. J. R€ uhli, MD, PhD, Institute of Evolutionary Medicine, University of Zurich, Winterthurerstr. 190, 8057 Z€ urich, Switzerland. Fax: 141446350112. E-mail: [email protected] Received 16 January 2015; Accepted 30 January 2015. DOI 10.1002/ar.23150 Published online in Wiley Online Library (wileyonlinelibrary. com).

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Fig. 1. Corresponding MR and CT image of skull region of an ancient Egyptian dog mummy; 1: signal intense structure in tongue area especially visible in MR image (ca. 100 BC; Collection of Animal Hospital University of Zurich, Switzerland; images: H. von Waldburg; Institute of Anatomy, University of Zurich).

tissue that has been thawed was successfully imaged by MRI (Notman and Aufderheide, 1995; R€ uhli et al., 2006) as well as ancient bog bodies (Bourke, 1986). State-of-theart use of clinical and nonclinical magnetic resonance techniques In a recent novel approach—without rehydration of the specimens—one was able to successfully apply nonclinical MR technology to show the spatial distribution of 1H and 23Na (2D and 3D 1H spin-echo projections; 2D 23Na solid-echo projection) in historic mummified human body parts. The body part studied was an isolated finger. The technical specifics of the analysis included a high-field small animal MRI System; internal resonator diameter about 2 cm; echo time about 800 ls, T2 about 300 ls; field of view as small as 27 3 27 mm2, with maximum spatial resolution up to about 120 lm (M€ unnemann et al., 2007). To better assess the topographic distribution of these chemical nuclei, a validating colocalization with clinical high-resolution MSCT has been done, showing the dissimilar distribution of 1H and 23Na. Sodium is of particular interest in research on ancient Egyptian corpses since it is the main chemical component of the natron-based antique artificial mummification techniques. The chemical differences of these nuclei require specifically adjusted MR settings such as imaging sequences, echo times (TE) or repetition times

(TR). However, this new methodological approach of 3Dassessement of chemical elements will allow better exploration of the impact of taphonomy as well as post mortem artificial treatment—as practiced in ancient mummification techniques—on human tissue morphology. For example, it may be applied in ongoing research efforts on adequate post mortem tissue conservation by visualizing in high-resolution the depth of the penetration of preservation agents or the specific alteration of size and shape of different anatomical compartments. Another study exploring a single mummy organ only, showed similar attempts by using fast imaging techniques on an isolated ancient mummified brain, specifically focusing on possible adipocerous formation observed (Karlik et al., 2007). By mean of a 1.5 T MR scanner and with small surface coils (diameter 7.6 cm) T1-weighted images only could be obtained. However, in combination with biopsies taken and examined by conventional histology and also by 31P, 23Na, and 1H MR-spectroscopy, some preliminary information about the organ—still containing bound water in a considerable amount—was recovered (Karlik et al., 2007). Apparently, transverse relaxation time (T2) is short in dry historic tissues and also most mummy samples would not fit in a conventional high-field magnet. However, by means of an open single-sided mobile,

MRI OF ANCIENT MUMMIES

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Fig. 2. MR-based 3D-reconstruction (left) of head region of a naturally mummified Peruvian corpse (right; ca. 1100 AD; Museum of History and Ethnography, St. Gall, Switzerland; MR image: H. von Waldburg, Institute of Anatomy, University of Zurich; Photograph: H. Sonderegger, Institute of Anatomy, University of Zurich).

R 5 MObile Univernotebook-sized appliance, the MOUSEV sal Surface Explorer (Bl€ umich, 2000) tissue differentiation can be conducted in superficial regions of historic bones and mummies (R€ uhli et al., 2007b). It may be possible to derive information about the preservation of bone structure in general from the obtained signals, but more research on this field is necessary. This technique recently allowed analyzing close-to-surface historic tissues in both temporal and spatial high resolution. As an example, the subcutaneous tissue layers of the Iceman mummy as well as the temporal alterations of his epicutaneous ice thickness, both of which may help to monitor his conservation in the future, were successfully recorded in situ inside the cold storage room (R€ uhli et al., 2007b). Highresolution spatial depth profiles with a resolution of up to 5 lm can be achieved with a multi-echo sequence (TE as short as 35 ls) allowing discriminating anatomical layers in wet or dry tissues, bone density signals or thin textiles such as bandages. Recently, the diagnostic value of standard clinical MR technique for spatial discrimination of historic dry tissues without rehydration was shown thanks to a newly available MR pulse sequence (R€ uhli et al., 2007a,c). It is possible to analyze 1H-signalbased images of soft tissues, bones, and embalming materials by using a so-called 3D-ultra-short echo time technique (UTE; echo time as short as 70 ls; spatial resolution of up to 0.8 mm; Nielles-Vallespin et al., 2007) as shown in ancient Peruvian and Egyptian mummies (up to 1500 BC; R€ uhli et al., 2007c). Especially, subchondral bone and collagen type 1 rich tissues are clearly visible. Also, recently the feasibility of clinical MR technology for spatial ancient frozen tissue differentiation, as in the Iceman glacier mummy (R€ uhli et al., 2006) has been shown; the large amounts of epicorporal and intracorporal hydrogen freely movable after thawing makes this feasible.

Compared to computed tomography (CT) images, MR proton signal images of dry ancient mummies have a higher signal-to-noise ratio (Figs. 1 and 2). Embalming substances, among others, show a greater signal variation in the MR than in the CT images, allowing an improved analysis of chemically diverse materials. Also, the MRI acquisition time (TA; often with multiple averages) can take from minutes to several hours. Ongoing evaluation of various MR techniques in ancient mummy imaging shows both, the impact of various pulse sequences (3D radial; single point imaging, 3D FLASH) as well as field strength (1.5 T versus 3 T systems) on image quality (e.g., blurring of edge structures) as expressed by spatial resolution and signal-to-noise ratio (Bock et al., 2008). In such a study, for high-resolution spatial colocalization CT data sets shall be acquired (prototype volume CT system e.g., with flat panel detectors; spatial resolution ca. 100lm) and both complementary image modalities eventually merged. On the whole, MR-based examination of historic bones and mummies is still in its infancy. MR-images often show a low contrast-to-noise ratio but a high signal-tonoise ratio, making the interpretation of the signalvariable images very difficult and thus making further research necessary. Using the UTE-MRI approach, massive morphological alterations by invasive rehydration of the sample prior to imaging can now be avoided for dry mummy tissues, allowing imaging of dry tissues with extremely short relaxation times. Anatomical variations and pathological alterations, such as atherosclerotic lesions, intervertebral disc protrusion, or degenerative arthritis, can be examined both, qualitatively as well as quantitatively, now better than ever in dry ancient tissues completely noninvasively. Future applications may include repetitive noninvasive imaging of ancient mummies for conservation follow-ups or forensic tissue spatial

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discrimination in dry and frozen mummified corpses as recently reported by Panzer et al. (2013), where a modern body part has been mummified and subsequently analyzed by CT (Brilliance 40; sl 5 mm, pitch 0.474, 120 kV) and MR (Magnetom Avanto; sequences: IR, T1w, T2w, UTE) in an experimental study.

CONCLUSIONS Generally, noninvasive imaging of ancient tissues is of increasing interest in historic, palaeo-anthropological, and palaeo-pathological studies, with CT currently still being the diagnostic gold-standard for mummy studies (R€ uhli et al., 2004). The above highlighted MR-studies show the successful application and diagnostic validation of novel imaging methods on ancient specimens. This broadens the technological spectrum for studies on historic human soft and hard tissues. More differentiated— and partially even superior—tissue discrimination will be possible by MRI compared to CT in the future, offering detailed anatomical examination, for example, of ligaments. It is well known that soft-tissue in historic mummified remains shows radio-anatomical characteristics quite different from known clinical data. In ancient mummies, postmortem dehydration and decomposition often leads to folded skin, and soft-tissues often appear radio-opaque on CT (Baldock et al., 1994). Apparently, it also influences the hydrogen density and mobility and thus MR imaging properties such as relaxation times. Hitherto, only CT could differentiate such altered softtissue in historic remains. This desired increase in diagnostic evidence in historic samples could be gained de facto by the introduction of new imaging modalities, such as clinical and nonclinical MRI, which shall be validated with established diagnostic techniques, such as CT. For an enhanced spatial morphological assessment, one shall typically apply correlatively state-of-the-art CT techniques as well as non-clinical and clinical MRI tech€ niques as outlined recently by Ohrstr€ om et al. (2013). This includes, for example, clinical MR settings with ultra-short echo time sequences. Thus, a different type of partially superior spatial tissue discrimination in comparison with CT is possible. The increasing demand for a sustainable, ethically correct methodology in research on tissue of deceased individuals will particularly encourage application of such completely noninvasive diagnostic techniques, in general. In addition, the current, ongoing advances in noninvasive imaging technology may make invasive techniques, such as autopsies, often superfluous in the future. Based on such pioneering methodological validation studies, one will more easily be able to define unambiguous criteria for an improved transdisciplinary assessment of the alteration of historic human morphology by intra vitam and post mortem factors. Unfortunately, since the major drive for the development of new diagnostic techniques is, quite naturally, clinical practice, palaeoimaging studies most often can only adapt what becomes available rather than direct develop specifically dedicated technologies. A “risk-benefit” analysis of any particular method used to be undertaken is strongly recommended, thus addressing issues concerning its sustainability/noninvasiveness versus its diagnostic sensitivity and specificity for such specific study settings. Finally, any improvement in diagnostic soundness in ancient morphological

structures in anatomico-palaeopathological research contributes to common knowledge of the evolutionary history of humans as well as their health and disease. However, compared to benchmarks applied in modern medical research, the level of diagnostic accuracy and spatial tissue differentiation in historic mummies is not great, especially if one uses non-invasive radiological techniques alone. The lack of contemporary clinical information on the ancient samples as well as the nature of the tissue alterations are some of the restrictions. Therefore, the desire to achieve a high degree of diagnostic sensitivity and specificity is a key factor in choosing any type of methodological approach in studies on human historic morphology and pathology. Thus, the critical development of this unique transdisciplinary scientific discipline is heavily linked to the evolution of diagnostic, primarily radiological, technology too.

ACKNOWLEDGEMENTS The author want to thank Hendrik von Waldburg, Dr.med.vet., and Siemens medical solutions for supporting MR-Imaging.

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MRI OF ANCIENT MUMMIES Notman D, Anderson L, Beattie O Amy R. 1986a. Arctic paleoradiology: portable radiographic examination of two frozen sailors from the franklin expedition (1845-1848). Am J Roentgenol 347–350. Notman DN, Tashjian J, Aufderheide AC, Cass OW, Shane OC, 3rd Berquist TH, Gray JE Gedgaudas E. 1986b. Modern imaging and endoscopic biopsy techniques in Egyptian mummies. Am J Roentgenol 146:93–96. Notman DNH. 1983. Nuclear magnetic resonance imaging of an Egyptian mummy. Paleopathol Newsl 43:9. Notman DNH. 1986. Ancient Scannings: Computed Tomography of Egyptian Mummies. In: David AR, editor. Science in Egyptology. Manchester: Manchester University Press. p 251–320. Notman DNH, Aufderheide AC. 1995. Experimental Mummification and Computed Imaging. In: I World Congress on Mummy Studies. Tenerife: Museo Arqueologico y Etnografico de Tenerife. p 821– 828. € Ohrstr€ om LM, von Waldburg H, Speier P, Bock M, Suri RE R€ uhli FJ. 2013. Scenes from the past: MR imaging versus CT of ancient Peruvian and Egyptian mummified tissues. Radiographics 33: 291–296. Panzer S, Borumandi F, Wanek J, Papageorgopolou C, Shved N, Colacicco G, R€ uhli F. 2013. Modelling ancient Egyptian embalming: radiological assessment of experimentally mummified human tissue by CT and MRI. Skeletal Radiol 42:1527–1535.

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Piepenbrink H Frahm J. Hanse A. 1986. Nuclear magnetic resonance imaging of mummified corpses. Am J Phys Anthropol 70:27–28. R€ uhli F, B€ oni T, Perlo J, Casanova F, Egarter E, Bl€ umich B. 2007a. Magnetic resonance imaging of ancient human mummies. Am J Phys Anthropol S44:204. R€ uhli FJ B€ oni T. 1999. Aktuelle mumienforschung der arbeitsgruppe f€ ur klinische pal€ aopathologie, universit€ at z€ urich. Bull Soc Suisse D’anthrop 5:1–10. R€ uhli FJ, B€ oni T, Perlo J, Casanova F, Baias M, Egarter E Bl€ umich B. 2007b. Non-invasive spatial tissue discrimination in ancient mummies and bobes in situ by portable nuclear magnetic resonance. J Cult Her 8:257–263. R€ uhli FJ, Chhem RK B€ oni T. 2004. Diagnostic paleoradiology of mummified tissue: interpretation and pitfalls. Can Assoc Radiol J 55:218–227. R€ uhli FJ, Egarter-Vigl E, Gostner P. 2006. First ever multislice CT and magnetic resonance imaging of the iceman, ca 3300 BC. Am J Phys Anthropol S42:156. R€ uhli FJ, von Waldburg H, Nielles-Vallespin S, B€ oni T Speier P. 2007c. Clinical magnetic resonance imaging of ancient dry human mummies without rehydration. JAMA 298:2618–2620. Sebes JI, Langston JW, Gavant ML Rothschild BM. 1991. Magnetic resonance imaging of growth recovery lines in fossil vertebrae. Am J Roentgenol 157:415–416.

Short Review: Magnetic Resonance Imaging of Ancient Mummies.

Noninvasive imaging of ancient tissues is of increasing interest in palaeopathological studies, with conventional X-ray and computed tomography curren...
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