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Figure 3. Normal Foot Anatomy
Pathology in the Royal Mummies
Tutankhamun's mummy was examined several times radiologically.20-23 Our inspection of the skull and trunk did not reveal novel information, but detailed examination of the king's feet yielded new data. Compared with the normal anatomy of the foot (Figure 3), the right foot had a low arch (Rocher angle, 132°; normal value, 126°). The medial longitudinal arch of the left foot was slightly higher than normal (Rocher angle, 120°) (Figure 4A), with the forefoot in supine and inwardly rotated position akin to an equinovarus foot deformity (Figure 4B). There were no pathological findings on the bone structure of the right metatarsal heads (Figure 5A). In contrast, the left second metatarsal head was strongly deformed and displayed a distinctly altered structure, with areas of increased and decreased bone density indicating bone necrosis (Figure 5B). The study further showed a widening of the second metatarsophalangeal joint space, with a normal articulating surface of the proximal phalanx. The third metatarsal head was only slighty deformed; the bony structure, however, showed signs of bone necrosis. The remaining left metatarsal heads appeared to be of normal structure (Figure 5B). The plantar surface of the left second metatarsal head shows a crater-shaped bone and a soft tissue defect in the area of bone necrosis (Figure 5C). The second and third toes on the left foot are in abduction. The second toe is shortened because it lacks the middle phalanx (oligodactyly [hypophalangism]). The proximal phalanx directly articulates with the distal phalanx (Figure 5D).
Infectious Diseases
Various infectious diseases are suspected or known to have been prevalent in antiquity,24-27 and some are described in remarkable detail in Egyptian papyri (eg, Papyrus Ebers, circa 1520 BC). Positive results were not found for pandemic plague (Black Death, bubonic plague), tuberculosis, leprosy, or leishmaniasis, but we identified DNA of P falciparum (the malaria parasite) in several of the royal mummies. Amplification of the P falciparum STEVOR gene family28 repeatedly yielded 149-bp and 189-bp amplicons for Tutankhamun and the TT320-CCG61065 mummy and also yielded a faint PCR band using DNA of the Yuya mummy. This result was replicated in further PCRs using DNA from other biopsies.
Figure 4. Analysis of Malformations in the Feet of Tutankhamun
Kinship Determination
More than 55 bone biopsies were used to elucidate the individual relationships of 18th-dynasty individuals, with the result that several of the anonymous mummies or those with suspected identities are now able to be addressed by name. These include KV35EL, who is Tiye, mother of Akhenaten and grandmother of Tutankhamun, and the KV55 mummy, who is most probably Akhenaten, father of Tutankhamun (Figure 2, eAppendix, and online interactive kinship analysis and pedigree). The latter kinship is supported in that several unique anthropological features are shared by the 2 mummies and that the blood group of both individuals is identical.31,32
Disease or Amarna Artistic Style?
Macroscopic and radiological inspection of the mummies did not show specific signs of gynecomastia, craniosynostoses, Antley-Bixler syndrome or deficiency in cytochrome P450 oxidoreductase, Marfan syndrome, or related disorders (eAppendix, Table 2). Therefore, the particular artistic presentation of persons in the Amarna period is confirmed as a royally decreed style most probably related to the religious reforms of Akhenaten. It is unlikely that either Tutankhamun or Akhenaten actually displayed a significantly bizarre or feminine physique.
It is important to note that ancient Egyptian kings typically had themselves and their families represented in an idealized fashion. A recent radiographic examination of the Nefertiti bust in the Berlin Museum illustrates this clearly by showing that the original face of Nefertiti, present as a thin layer beneath the outer surface, is less beautiful than that represented by the artifact.33 Differences include the angles of the eyelids, creases around the corners of the mouth on the limestone surface, and a slight bump on the ridge of the nose.34 Thus, especially in the absence of morphological justification, Akhenaten's choice of a “grotesque” style becomes even more significant.
Walking Impairment and Canes
Tutankhamun had a juvenile aseptic bone necrosis of the left second and third metatarsals (Köhler disease II, Freiberg-Köhler syndrome). The widening of the metatarsal-phalangeal joint space, as well as secondary changes of the second and third metatarsal heads, indicate that the disease was still flourishing at the time of death.35 Bone and soft tissue loss at the second metatarsal phalangeal articulation could further indicate that an acute inflammatory condition was present on the basis of an ulcerative osteoarthritis and osteomyelitis. The congenital equinovarus deformity (pes equinovarus) together with the malformed second toe of the left foot (oligodactyly [hypophalangism]) transferred additional joint load to the right foot, causing flattening of the foot arch (pes planus).
There is evidence that Tutankhamun may have had this impairment for quite some time. The walking disability can be substantially aided by the use of a cane. Howard Carter discovered 130 whole and partial examples of sticks and staves (eFigure 3A) in the king's tomb, supporting the hypothesis of a walking impairment.36 Traces of wear can be seen on a number of the sticks, demonstrating that they were used in the king's lifetime (eFigure 3B). Additional evidence for some sort of physical disability is found in a number of 2-dimensional images from Tutankhamun's reign that show him seated while engaged in activities for which he normally should have been standing, such as hunting (eAppendix and eFigure 3C).37,38
Figure 5. Analysis of Pathology in the Feet of Tutankhamun
Malaria Tropica
Macroscopic studies revealed areas of patchy skin changes on the pharaoh's left cheek and neck of uncertain anamnesis, possibly indicating an Aleppo boil, a plague spot, an inflamed mosquito bite, or a mummification artifact.39 However, the genetic identification and typing of plasmodial DNA in Tutankhamun, Thuya, Yuya, and TT320-CCG61065 showed that they must have had malaria tropica, the most severe form of malaria (eAppendix).
Literary evidence for malaria infection dates back to the early Greek period, when Hippocrates described the periodic fever typical of this disease.40 Although it is believed that malaria widely affected early populations before Hippocrates,27,41 until now only 1 report using immunological tools42 and few molecular genetic studies have clearly identified P falciparum in ancient specimens.43-46 We not only identified this parasite in our sample but also observed individual differences in some of the gene sequences as well as different MSP1 allele constellations in the 4 positive mummies. The diversity of plasmodial DNA (ie, variability in the genes' base order, length polymorphisms, or both) is a well-known phenomenon; however, some of the base deviations were not found in current DNA databases. Further research is required to typify these alterations in more detail and to assign these potentially unknown patterns to ancient Egyptian Plasmodium strains that date back to 3300 to 3400 years before present.
Figure 6. Identification of Plasmodial DNA in 18th-Dynasty Mummies
Cause of Death
Caution must be taken when interpreting cause of death in these mummies. It can be speculated that Yuya and Thuya had malaria, but it is not known if this was lethal (Table 3). Surprisingly, both individuals had reached an advanced (for the time) age of approximately 50 years or older (Table 1). This means either that the infection took place quite late in their lifetime, that they enjoyed strong genetic fitness, or that they aquired a partial immunity against the pathogen during their lives. Not every person infected with P falciparum becomes gravely ill, and this is especially true in populations that have been exposed to malaria pathogens over long periods.52 If Yuya and Thuya spent much of their time living in malaria-endemic areas close to the marshes of the Nile River, partial immunization may have contributed to their survival.
On the other hand, Tutankhamun had multiple disorders, and some of them might have reached the cumulative character of an inflammatory, immune-suppressive—and thus weakening—syndrome (Table 3). He might be envisioned as a young but frail king who needed canes to walk because of the bone-necrotic and sometimes painful Köhler disease II, plus oligodactyly (hypophalangism) in the right foot and clubfoot on the left. A sudden leg fracture23 possibly introduced by a fall might have resulted in a life-threatening condition when a malaria infection occurred. Seeds, fruits, and leaves found in the tomb, and possibly used as medical treatment, support this diagnosis (eAppendix, eFigures 3D and 3E).24,25,53-57
In conclusion, this study suggests a new approach to research into the molecular genealogy and pathogen paleogenomics of the Pharaonic era. With additional data, a scientific discipline called molecular Egyptology might be established and consolidated, thereby merging natural sciences, life sciences, cultural sciences, humanities, medicine, and other fields.
JAMA. 2010;303(7):638-647. doi:10.1001/jama.2010.121
