MUMMIES / LES MOMIES Diagnostic paleoradiology of mummified tissue: interpretation and pitfalls Frank J. Rühli, Dr. med., PhD; Rethy K. Chhem, MD, PhD, FRCPC; Thomas Böni, MD D ead human and animal tissue can, because of natural conditions or artificial attempts, escape postmortem decay partially or even completely. This process called “mummification” derives linguistically from the Persian word mum or mom, which means beeswax.1 In order to conduct an accurate radiologic diagnosis of the anatomical and pathologic changes in mummies, and thereby advance research in this area, a thorough knowledge of the process of mummification itself is required. The purpose of this article is to review the role of diagnostic paleoradiology in mummy studies. Natural mummification may occur under contrasting climatic conditions: the alpine/arctic process of freeze-drying, which requires sufficient air flow to sublimate body water; preservation in northern European peat bogs, in which acids interfere with enzymatic soft-tissue decomposition; or the mummification that can happen in the hot and arid environment of deserts. Artificial mummification can be achieved by embalming a body, as seen in the funerary tradition of Ancient Egypt where a physically wellpreserved body was essential to gain immortality. Surprisingly, this method has been described very rarely in historical times and is passed on to us de facto only by Herodotus of Halicarnassus (fifth century BC) and by Diodorus Siculus (first century BC). Essentially, it involved the complete or incomplete removal of the internal organs using diverse tools.2 Desiccation of the body was obtained by using natron,3,4 a blend of NaCl, Na2CO3, NaHCO3 and NaP2SO4.5 The term “natron” was coined after the Wadi Natrun region in Egypt. The embalming substance was a still mostly unknown mixture of natron with various preserving and aromatic products.6–12 Finally, the corpse was wrapped with bandages and kept within a coffin in a well-sealed tomb. Since antiquity, the presence of valuable burial goods, such as jewellery and religious objects, in Egyptian tombs has attracted many thieves. Mummies recovered in modern times usually bear several stigmata of these acts of vandalism caused by tomb looters. Burial artifacts have also been removed during archaeological excavations and the scientific unwrapping of mummies. Mysterious deaths of scientists have been linked with the “curse of the Pharaohs,” a romantic speculation without any strong scientific basis.13 Postmortem alterations of soft tissues and bone caused by artificial mummification are numerous. Internal organs were either removed completely and kept in jars or were put back in the abdominal cavity after being embalmed separately. The latter were also called “organ packages” to differentiate them from packed rolls of bandage that were used to fill the empty body cavities. Rarely, bones were macerated and the soft tissue remodelled using layers of mud.14 During the 21st dynasty (ca. 1000 BC) in Ancient Egypt, the skin was incised at various locations and layers of mud were inserted subcutaneously to make the skin appear livelier. Often, the brain was removed through the ethmoidal cells and cribriform 218 JACR VOL. 55, No 4, OCTOBRE 2004 Rühli, Böni — Clinical Paleopathology Team, Orthopedic University Clinic Balgrist and Institute for the History of Medicine, University of Zurich; Rühli — Institute of Anatomy, University of Zurich, Zurich, Switzerland; Chhem — Paleoradiology Research Unit, Department of Radiology, London Health Sciences Centre, University of Western Ontario, London, Ont. Address for correspondence: Dr. Frank J. Rühli, Institute of Anatomy, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland; fax 4116355702; [email protected] Submitted Mar. 1, 2004 Accepted May 19, 2004 Can Assoc Radiol J 2004;55(4):218-27. © 2004 Canadian Association of Radiologists PALEORADIOLOGY OF MUMMIFIED TISSUE plates,15,16 without clear preference for a particular nostril side.17 All organs of human bodies are significantly altered because of the taphonomic processes observed in mummification. The skin usually loosens from the epidermis. Body hair is rare,18 because it may have been shaved at the beginning of the embalming process. In the naturally frozen mummies of the High Andes, postmortem alterations have been recently evaluated in some detail by Previgliano et al19,20 using a nonhelical computed tomography (CT) scanner. These authors showed a decrease in size of soft-tissue compartments resulting from the loss of water during the natural process of mummification. However, the overall state of preservation of these bodies remains excellent and allows an accurate identification of internal organs and soft-tissue pathologies. Finally, experimental mummification of human4,21 and animal remains22,23 has been performed in modern times as well, generally showing radiologic and anatomical features comparable to those demonstrated in authentic ancient mummies. RADIOLOGIC INVESTIGATION OF MUMMIES The earliest radiologic examinations of mummies were performed by Koenig,24 Holland25 and Dedekind,26 within a few months of the discovery of x-rays by Roentgen,27 and later by Petrie.28 Conventional radiologic assessment of mummies has been an established diagnostic tool for decades.29 The technical protocol and parameters used in conventional radiographic studies of mummies have been described before.6,20,30,31 Furthermore, CT has been used as an adjunctive, noninvasive modality to radiography for the investigation of mummies, including the establishing of the presence of bones within a wrapped bundle32 or the identification of embalming artifacts inserted during the wrapping process.33,34 The respective role of conventional radiography, CT and magnetic resonance imaging (MRI) for fossil studies, in particular, has also been reviewed.35 Finally, the value of CT in the clinical assessment of skeletal pathologies in the modern population has been well established.36 The method of interpretation of radiologic features for detecting diseases in modern clinical situations has often been applied to the diagnosis of paleodiseases. Radiopathologic findings in clinical situations should be compared with those in ancient tissues with extreme caution, because the features of contemporary disease may have been altered by modern treatment such as antibiotics, steroids, radiation therapy or chemotherapy. Furthermore, ancient remains may show conditions that are no longer present and known in our times. To increase the accuracy with which paleopathologic conditions can be detected and, therefore, to minimize diagnostic errors, the images should be preferably acquired, analyzed and interpreted by experienced radiologists in collaboration with either a physical anthropologist or a pathologist specialized in the study of ancient remains. The best method with which to approach the investigation of ancient skeletal remains would be similar to that of a clinical “tumour board” where a skeletal radiologist, orthopedic surgeon and bone pathologist meet to discuss radiologic and pathologic findings. Most of all, there is still no acceptable reference standard for paleopathologic diagnosis. Yet, conventional radiography remains the essential foundation of the diagnosis of disease in mummies. It has many advantages, including wide availability, easy access, low cost and, most important, high spatial resolution. Unfortunately, its low contrast resolution may sometimes prevent the researcher from making an accurate distinction between mummified soft tissue and embalming artifacts. The superimposition of various body parts because of a mummy’s positioning37 and the presence of wooden coffins (Fig. 1), wrapping materials, embalming substances and radio-opaque amulets represent major limitations for an adequate interpretation of the x-ray films because of the artifacts they create (Fig. 2).6,30 Fluoroscopy and spot radiographs have also been used as screening tests for possible imaging pitfalls in the initial investigation of mummies.30 With the use of digital FIG. 1: Conventional radiograph (dorsoplantar direction from inside the coffin) of the feet of an Ancient Egyptian mummy (ca. 300 BC ; Naturwissenschaftliche Sammlungen, Winterthur, Switzerland) with radio-opaque artifacts resulting from the presence of nails and lead-based colour paintings on a modern sarcophagus (Post-Napoleonic Egyptomania style, late 18 th to early 19th century AD). CARJ VOL. 55, NO. 4, OCTOBER 2004 219 RÜHLI ET AL radiography, as recently introduced in clinical practice, some of these pitfalls may not be a problem any more. CT easily suppresses superimposition. Its ability to measure the densities of mummified tissues may bring additional information about diseases, the embalming process and other postmortem alterations (Table 1).6,38–44 The radiologic investigation of the approximately 5300-year-old Copper Age natural mummy called the “Iceman from Tyrol” shows how much imaging contributes to the diagnosis of paleopathologies.45–47 In that case, diagnostic paleoradiology detected healed rib fractures; premortem stress markers (e.g., Harris lines); arteriosclerosis, as reported in other mummies;34,48–53 and anatomical variations such as bilateral absence of ribs, osteoarthritis of feet, an arrowhead in the left shoulder region and postmortem skeletal changes. There are numerous potential radiologic pitfalls when investigating Egyptian mummies. The process of embalming leads to some typical alterations that can be detected on CT. Postmortem dehydration and decomposition produces irregular folded skin appearing as multiple layers of dry, soft tissues, separated by air pockets. Furthermore, in some cases, soft tissues are more radio-opaque,5 possibly because of shrinkage and deposition of embalming materials/wrappings. Therefore, the differentiation of a mummy’s abdominal organs can be very difficult.37 The matrix between the bone trabeculae is often replaced by air, therefore becoming more radiolucent, whereas shrunken parenchymatous organs turn more radiodense.39 By comparing an initial CT examination and one performed 2 years later, Murphy et al47 showed a change in trabecular bone feature and density, with a different pattern of airspace distribution in the medullar cavity. It is not clear whether this phenomenon was induced by an air–ice exchange during the taphonomic process or not. Mummies’ brains can display a varied degree of preservation, as shown in conventional x-ray films of bodies that have been preserved in peat bogs.54 When a brain is still left in situ, it is sometimes, but not always, possible to differentiate grey matter from white matter on computed tomographic images.19,20,47,55,56 The presence of residual meningeal linings has been interpreted as an evidence for the lack of an attempt to remove the brain post mortem in such an individual.17 However, these meningeal layers can be found even when the brain is completely removed and, therefore, should not be used as an indicator for brain preservation (Fig. 3).33 Those intracranial artifacts may simulate authentic lesions, and awareness of these problems is of the utmost importance to prevent a wrong diagnosis of cerebral pathologies in mummies. A B DIAGNOSTIC PALEORADIOLOGY: RADIOLOGIC FEATURES, PATHOLOGIC ANATOMY AND ARTIFACTS FIG. 2: Conventional anteroposterior radiograph (left) and computed tomographic (CT) image (right) of the abdominal region of an Egyptian mummy (ca. 900 BC; Musée d’ethnographie, Neuchâtel, Switzerland; CT data: Somatom HiQ scanner [Siemens, Erlangen, Germany], 133 kV, 120 mA) show multiple opacities, representing embalming substances, intra-abdominal stuffing and wrapping materials. 220 JACR VOL. 55, No 4, OCTOBRE 2004 PALEORADIOLOGY OF MUMMIFIED TISSUE Postmortem alterations of the anatomy of the chest and collapsed lungs make radiologic interpretation in mummy studies often extremely difficult, as seen in the Iceman mummy where snow and ice pressure led to a severe anteroposterior collapse of the entire thorax.47 In another case, a diagnosis of air-inflated lung tissue was suggested by CT, but autopsy showed frozen pleural fluid as part of a hemopneumothorax.52 In the same study, radio-opaque masses located in the left side of the abdominal cavity were coprolites and not “organ packages,” as confirmed by autopsy of the corpse. Postmortem fractures are commonly seen in the pelvic girdle and the spine. Rib fractures may be caused by postmortem trauma caused by excessive wrapping with bandages of an Egyptian mummy.51 It is not unusual to identify vertebrae51 or teeth in a wrong anatomical location in Ancient Egyptian mummies.6 Intervertebral disc spaces are smaller30,47 in mummies because of desiccation. They may contain air as a result of the postmortem alterations6 and, in some instances, ochronosis-like pigmentation may occur. In contrast to earlier claims of possible alkaptonuria,57 Walgren et al58 used MRI spectroscopy to confirm that substance deposition in intervertebral discs was instead most probably induced by the embalming process itself. Braunstein et al59 reported chondrocalcinosis of intervertebral disc and menisci as a possible embalming artifact. Finally, for Gray,60 the calcification of the intervertebral disc in mummies is the result of natron deposition within the intervertebral disc. Embalming substances can be found all over a mummy’s body, especially in the anatomical cavities, mainly the thorax, abdomen, external auditory canal and orbits. Resin, in particular, has been identified in bone61 and joints.62 FIG. 3: CT image shows an empty mummy skull (ca. 900 BC; Musée d’ethnographie, Neuchâtel, Switzerland; CT data: Somatom HiQ scanner [Siemens], 133 kV, 120 mA) with dura mater remains, which are especially visible as they are attached at the tabula interna on the right temporal side, despite obvious postmortem removal of the brain through the left ethmoid region. There are deposits of residual high-density embalming substance in the middle. Bilateral eye-like decorations are visible. Table 1: Density* of mummification-related structures established by computed tomography Structure Lung Various bones (some areas with an air-filled matrix of spongiosa) Density, Hounsfield units (HU) –920 –638 to 953 Reference Sigmund and Minas38 Rühli6 Ocular bulb filling –600 Sigmund and Minas38 Air-filled artificial subcutaneous space –543 Rühli6 Soil (subcutaneous stuffing material) –150 Hübener and Pahl39 Beeswax –140 Hübener and Pahl39 Ointment–oil 40 Germer et al40 Resin-like fluid 71 Sigmund and Minas38 Various embalming materials (grains/solid) Artificial eye (various materials) Plaster Ceramic toe prosthesis Gold 430/773/1148/1427 523/525/2251/2346/2422 1000 –600 to 1318 > 1500 Soto-Heim et al41 Baldock et al5 Hübener and Pahl39 Wagle42 Hübener and Pahl39 Amulet 1600 Sigmund and Minas38 Calcium carbonate repair 1828 Rühli,6 Rühli and Böni43 Heart scarab† 2410 Jansen et al44 *Reference HU values: air, –1000 HU; water, 0 HU; soft tissues, about –100 HU to 100 HU; bone, about 500 HU to 2000 HU. †An important amulet that was usually placed in the mummy wrapping. CARJ VOL. 55, NO. 4, OCTOBER 2004 221 RÜHLI ET AL COMPUTED TOMOGRAPHIC INVESTIGATION OF MUMMIES Although guidelines for the examination of nonclinical skeletal material by CT have been validated,36 the accuracy and reliability of CT in the investigation of mummified tissues has yet to be established. Current CT protocols for mummy investigations are listed in Table 2.17,44,48,63–65 For Rubinstein et al,66 the ideal protocol for CT of mummies should provide the “thinnest slice, the highest spatial resolution rather than contrast resolution, and a low radiation dose,” which is similar to the protocol suggested earlier by Ruff and Leo.36 In addition, initial scout view images in main planes are important to determine whole-body CT planning, and it is also critical to choose adequate parameters to protect the thermal capability of the x-ray tube.48 The quality of computed tomographic imaging67 in the radiologic–anatomical assessment of mummies has drastically improved since its earliest application about 25 years ago.55,68–70 It is now possible to use CT to investigate small anatomical structures such as the middle and inner ear of a mummy.17,71 High-resolution CT has much improved since its early use in the study of hominoid fossils.72 Large, single trabeculae can be visualized, and quantitative measurements of anatomical landmarks, linear and angular dimensions, as well as cross-section area and volume calculations can be assessed. Micro-CT73 enables the study of the microanatomy of bone architecture with a spatial resolution of a few micrometres. However, only small sample diameters of a few centimetres can be scanned. Current state-of-the-art CT post-processing tools include both multiplanar reformatting (MPR) and 3dimensional (3D) volume-rendered, shaded-surface display17,37,44,48,63 of multislice CT (MSCT)74 images in mummy research44,48 that allow faster acquisition and improved data after processing. The advantages of radiography, single-slice CT and MSCT for the investigation of ancient human skeletal remains have been reported in the literature.75,76 Shorter data acquisition time would theoretically be critical for studies of frozen mummies, because they need to be sent back to the freezer within a few minutes.19,20 MSCT also allows a single acquisition of volume data for a whole body and a reconstruction of a whole mummy without much difficulty.48 On the other hand, most MSCT protocols produce a huge stack of CT images, between 1000 and 1200 for a mummified whole-body scan.48,63 Fortunately, protection of the specimen from radiation is not an issue77 for radiology as practised on ancient human skeletal remains, except its possible impact on subsequent ancient DNA examination.78 3D CT has been applied to mummies79–83 mainly to conduct a virtual unwrapping,5,7,17,37,40,44,48,63,84,85 to identify internal anatomy,17,48,63,82,86 to detect pathologies,17,87,88 and to calculate endocranial capacity89 or craniometric indices.48 These reconstruction techniques allow a geometric assessment of wrappings, confirm the presence of wads of stuffing, display the mummy’s hairstyle, help evaluate a cranial bone fragment as associated with a cause of death, depict subtle postmortem soft-tissue lesion of an ear or the base of the skull, and help assess the status of brain and intestine removal.16,63 3D CT has also provided a precise image of a cleft lip in a child’s mummy17 and has been used to measure the precise stature of mummies.48 When, in occasional cases, a wooden stick was inserted into the spinal canal during the process of embalming, CT then has helped to deter- Table 2: Exemplary protocols for computed tomographic studies of mummies Structure (no. of examples) Imaging protocol Whole body (n = 13) 2.5-mm slice thickness, 1.25-mm reconstruction interval, 120 kV, 140 mA Cesarani et al48 Skull (n = 13) 1.25-mm slice thickness, 0.7-mm reconstruction interval, 120 kV, 140 mA Cesarani et al48 Whole body (n = 9) 3-mm slice thickness, 120–140 kV, 70–100 mA Hoffman et al63 Skull/upper cervical spine (n = 9) 1-mm slice thickness, 120–140 kV, 70–100 mA Hoffman et al,63 Hoffman and Hudgins17 Head/neck (n = 25) 1-mm slice thickness, 0.7-mm reconstruction interval, 120 kV, 100 mA Jansen et al44 Trunk/legs (n = 25) 3-mm slice thickness, 2-mm reconstruction interval, 120 kV, 200 mA Jansen et al44 Whole body (n = 1) 2.5-mm slice thickness, 2.5-mm reconstruction interval, 120 kV, 210 mA Shin et al64 Skull (n = 1) 2.5-mm slice thickness, 2.5-mm reconstruction interval, 120 kV, 160 mA Shin et al64 Scarabs (n = 9 in 25 mummies) 0.5-mm slice thickness, 0.3-mm reconstruction interval, 120 kV, 135 mA 222 Reference JACR VOL. 55, No 4, OCTOBRE 2004 Jansen et al65 PALEORADIOLOGY OF MUMMIFIED TISSUE mine its location and the status of the spine itself.7,48 Dental attrition in mummies can also be assessed.90 Finally, the state of preservation of teeth48 has been evaluated using orthopantomographic or orthoradial 2D CT.91 Stereolithographic modelling of mummies,92 designed from 3D computed tomographic data, still has its drawbacks because of high costs and being a timeconsuming procedure,92 as well as the lack of accuracy due to the partial volume effect.35,47,93,94 Weber et al95 established an overall 2% error in the accuracy of computed tomographic measurement of the endocranial volume of hominid skulls. Recheis et al96 determined the error of measurement for stereolithographic models to be 0.5 mm in each dimension. Finally, Hjalgrim et al92 described a technical accuracy of 0.1 mm. Overall, the impact of stereolithographic models in evaluating mummies and skeletal human remains is better than the 2D CT study only.94,96 The study of 3D CT in mummy facial reconstruction97 is beyond the scope of this paper. Virtual endoscopic “fly-through” and “autostereoscopic display” have proved useful in the investigation of human remains.48,63,96 Invasive endoscopy can give good insight into a mummy’s body cavities, usually by going through artificial or postmortem created holes. 6,34,61,98–100 In some selected cases, computerassisted101,102 and CT-guided biopsy103 are useful tools for the assessment of internal structures within an unwrapped mummy. However, the performance of these procedures is difficult because of the hard and dry mummified tissue.98,103,104 Using x-rays100 or, better, CT guidance,103 the region of the biopsy can be better located. The CT display window setting is important too, because it helps identify anatomical and pathologic structures in mummies. An all-purpose proposal for these parameters cannot be outlined here. However, usually a “soft-tissue” window setting produces better contrast for mummified tissues than the bone windows. Further research is required to confirm this empirical observation. Computed tomographic density measurement of an unknown structure can help with its identification, because the chemical components are reflected by their attenuation values (Hounsfield units [HU]) (Table 1).5,41 A correlation between computed tomographic features and densities and the historical context is crucial for the interpretation of the images.6,43 In addition, the density (HU) must be interpreted more cautiously at the edge of a mass, and the possible presence of beamhardening artifacts should be considered.36 The assessment of the mineral content of a mummy’s skeleton has not yet been completely explored. It has been demonstrated that the embalming process interferes with the normal mineral content in human bones and creates artificial results of unclear significance.82 Assessment of the mineralization of a mummy’s toe has been performed that has provided evidence to support the hypothesis of its distal amputation during the individual’s life.53 Tissue demineralization and taphonomic encrustations of minerals may actually affect CT resolution,96 as was observed for the Iceman. Specific algorithms may help in dealing with encrustations in fossils96 and improving morphological analysis. These technical issues have been reviewed in human evolutionary studies.35 Software that corrects for metal artifacts has been used to prevent pitfalls consisting of metallic artifacts that are caused by high-density structures such as amulets.82 The density of nonorganic artifacts found in Egyptian mummies has also been studied.5 CT has also been used to identify and localize burial goods inserted within the corpse or included in the wrappings during the mummification process. These amulets (e.g., scarabs) are found in more than one-third of all mummies44 and, with the application of MPR, it is even possible to decipher the inscriptions on scarabs without the need for an unwrapping of the mummy itself.44 In some cases, CT has been used for an in-depth structural component analysis of famous Ancient Egyptian art.105 To conclude this section, the major advantage of computed tomographic imaging is the generation of digital data that can be stored, retrieved and shared easily using electronic media and kept as a database for a particular mummy.86 DETERMINATION OF SEX, AGE AND CAUSE OF DEATH: ROLE OF RADIOLOGY Age at death and sex can be difficult to determine in mummies, especially if they are still wrapped in bandages. Well-established anthropological methods for determining these characteristics are based on the assessment of dry bone and not on a mummy’s radiographic findings.30 Often the external and internal genitalia are no longer present in artificial mummies because of embalming practices and the mummies are, in addition, still wrapped. Cesarani et al106 were able to determine sex in 11 of 13 examined mummies, but others have had less accurate results.17,51 In one study, the penis of the mummy could be seen on radiographs, in contrast to the female painting of its sarcophagus.107 Braunstein et al59 were able to determine the sex of half of a series of 12 royal mummies using conventional radiography. In bog bodies, sex determination was not achieved in 35% of the sample.108 If the pelvic girdle is intact, radiography performed in “standardized” planes may be useful in the determination of sex. Furthermore, CTgenerated cephalometric data can be used to determine the sex of a mummy.109 Virtual CT reconstruction of intact pelvic bone may help too. To determine an individual’s age at death is difficult CARJ VOL. 55, NO. 4, OCTOBER 2004 223 RÜHLI ET AL as well. About 30% of a sample of bog bodies could not be linked to a particular age group.108 Various techniques have been used to overcome this major limitation and include the radiologic study of pubic bone, but done in macerated specimens only,110 anthropometric long-bone measurements20 or dentition assessment.5,20 However, even for the otherwise extremely well investigated Iceman, only a roughly estimated age of 40–50 years was achieved.47 There is so far no nondestructive test available that is accurate enough to become a reference standard for the determination of the age at death of mummies. Cause of death is also often difficult to diagnose because of, for example, problems in differentiating periand postmortem trauma. Many published radiologic studies fail to mention any cause of death.6,30,83,111,112 Only in exceptional cases can the cause of death be assumed, such as a rare mummified Roman who showed what would appear to be a bilateral fibrinous pleurisy that may have led to death.56 OTHER IMAGING MODALITIES FOR MUMMY STUDIES The absence of intracorporeal fluids results in a lack of image on MRI study.7,30,37,61,113–116 Notman et al61 used a body coil with multiple different scanning sequences but failed except for a free-induction-decay signal, which was too weak to generate an image. However, Piepenbrink et al113 were able to produce MR images with spatial resolution of 0.5 mm from rehydrated mummified tissue. Nevertheless, they stress the difference in such images from those obtained in clinical situations, especially the absence of lipid signals. The role of MRI in detecting lipid signal in a mummy’s residual fat-containing tissue has yet to be validated. The low cost of ultrasonography and its availability and portability made this modality a very appealing imaging method for mummy studies in the field. Unfortunately, the presence of air and embalming substances are major obstacles to the progression of an ultrasound beam that prevents the formation of acceptable images.39 Conventional x-ray arthroscopy of a knee joint has been performed in paleoimaging31 but remains anecdotal. CONCLUSION A thorough knowledge of the mummification process and radiologic pitfalls, such as artifacts, is essential for an adequate interpretation of x-ray films and computed tomographic images of mummies. Despite the high sensitivity in anatomy and lesion detection offered by CT, this imaging technique lacks the specificity that would make it the modality of choice for diagnostic purposes. 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