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ORIGINAL ARTICLE

Pathological skeletal remains from ancient Egypt: the earliest case of mellitus?

TL Dupras*, LJ Williams, H Willems, C Peeters

Introduction ABSTRACT The first accurate description of dia- The diagnosis of diabetes mellitus from skeletal remains is very difficult given the betes mellitus, attributed to Aretaeus complexity of the disease and the fact that there are no pathological skeletal of Cappadocia, appeared in ancient characteristics exclusively associated with diabetes mellitus. Skeletal identification of historical sources ca. 100 AD, though diabetes mellitus may only be possible through differential diagnosis, when several many credit the Ebers papyrus as pathological changes are present. Skeletal and dental changes associated with diabetes containing the earliest medical refer- mellitus include Charcot’s (neuropathic ), osteoporosis, , ence to the disease (see Table 1 for diffuse idiopathic skeletal hyperostosis (DISH, or Forestier’s disease), adhesive capsulitis milestones in the history of dia- (frozen shoulder), dental caries, periodontal disease, and antemortem tooth loss. betes).1–3 The Ebers papyrus, dated Skeletal remains of an adult male from the Egyptian archaeological site of to approximately 1530 BC, is one of Dayr al-Barsha, dated to the Middle Kingdom (ca. 2055–1650 BC), display a myriad of the oldest Egyptian medical docu- pathological conditions that, when considered together, likely indicate diabetes mellitus, specifically mellitus. ments and, although it contains over This diagnosis represents the earliest, and possibly the only recorded archaeological 700 magical spells and medical reme- skeletal evidence for this disease. Copyright © 2010 John Wiley & Sons. dies, it also contains phrasing that Practical Diabetes Int 2010; 27(8): 358–363 mentions a particular symptom indicative of diabetes mellitus.3–5 KEY WORDS The phrases ‘to eliminate urine diabetes mellitus; type 2 diabetes; diffuse idiopathic skeletal hyperostosis; which is too plentiful’ [EB 274] and brachydactyly; osteoporosis; Egypt; Dayr al-Barsha ‘to put the urine in order’ [EB 266] may be translated as referring to characteristics, consequently adding One individual’s skeletal remains polyuria, a classic symptom of to the difficulty of diagnosis. from the site of Dayr al-Barsha, diabetes mellitus. The Ebers papyrus Skeletal changes associated with Egypt, display a myriad of pathologi- also refers to ‘correcting urine of diabetes mellitus are not directly cal characteristics that, when consid- excess’ [EB264], which may be a caused by the disease itself, and are ered together, present a strong more likely reference to polyuria due most often seen as chronic long-term case for the diagnosis of diabetes to diabetes.3 Parallels to this descrip- complications associated with types 1 mellitus, and may represent the tion are also found in the later dated and 2 (early and late onset, respec- earliest and only published skeletally (18th Dynasty, ca. 1479 BC) Hearst tively). , on the identified archaeological case of papyrus [H63].4 other hand, is normally short term diabetes mellitus. One problem in tracing the his- (the length of the pregnancy) and tory of diabetes mellitus is that there usually does not lead to skeletal Skeletal/dental characteristics are no skeletal or soft tissue character- changes. Skeletal characteristics typi- of diabetes mellitus istics exclusive to diagnosis in the cally associated with chronic diabetes Adhesive capsulitis archaeological record; therefore, include adhesive capsulitis (frozen Adhesive capsulitis is an idiopathic paleopathologists have relied on tex- shoulder), diffuse idiopathic skeletal condition whose aetiology is not tual evidence to trace the appearance hyperostosis (DISH, or Forestier’s clearly understood; however, it has of this disease. If it is possible to iden- disease), Charcot’s joint (neuro- been reported as having a significant tify diabetes mellitus in skeletal pathic arthropathy) as part of the correlation with diabetes mellitus, remains, it can only be achieved complex, osteoarthritis, particularly type 2.6,14 The disease through differential diagnosis so that and osteopaenia/osteoporosis.6–10 appears to have a high prevalence in all potential diseases are considered. Diabetes mellitus also has a discern- individuals over 40 years of age and is Due to the pathogenic complexity of able association with dental caries, associated with the duration of dia- diabetes mellitus, individuals may periodontal disease, and ante- betes.14 Although the disease itself is present with several different skeletal mortem tooth loss.11–13 primarily found in the soft tissues of

TL Dupras, PhD Subfaculteit Taal- en Regiostudies, Central Florida, Orlando, FL 32816, USA; LJ Williams, PhD Katholieke Universiteit Leuven, Leuven, e-mail: [email protected] Department of Anthropology, University of Belgium Central Florida, Orlando, USA Received: 18 June 2010 H Willems, PhD *Correspondence to: Dr Tosha Dupras, Accepted in revised form: C Peeters, MA Department of Anthropology, University of 10 August 2010

358 Pract Diab Int October 2010 Vol. 27 No. 8 Copyright © 2010 John Wiley & Sons ORIGINAL ARTICLE Pathological skeletal remains from ancient Egypt: the earliest case of diabetes mellitus?

the shoulder, clinical radiographs Table 1. Milestones in the mellitus commonly show associated bony responses such as osteoporosis, Date Event degenerative arthritic changes, and osteophytic development in the 1530 BC Ebers Papyrus, Egypt – first mention of polyuria scapular glenoid cavity and the humeral head.15 100 AD Aretaeus of Cappadocia – first accurate description of the disease, and coined the term ‘diabetes’ (from the Greek Diffuse idiopathic skeletal ‘diabainein’) hyperostosis Diffuse idiopathic skeletal hyperosto- 1000 BC to 6th Susruta of India – first clinical diagnosis of diabetes sis is a pathological condition charac- century AD (date terised by ossification of the anterior of occurrence longitudinal ligament and ossifica- under debate) tions of other extra-spinal ligaments and entheses. Ossification of the 1300s AD Purgatives, and astringents prescribed by physicians to anterior longitudinal ligament is relieve intense polyuria mainly reported on the right side, and DISH is only diagnosed archaeo- 1675 AD Thomas Willis – added the word ‘mellitus’ (from the Latin of logically if there is contiguous fusion honey) to refer to the sweet taste of urine of four or more vertebrae.16 Even though it is mainly observed in the 1776 AD Matthew Dobson – confirmed that sugar was present in thoracic segment of the vertebral both the urine and blood of diabetic individuals column, DISH can occur in any area of the spine. Although the aetiology 1788 AD Thomas Cawley – discovered correlation between of DISH is not yet understood, it shrivelled pancreas and diabetic individuals appears to occur more frequently in individuals with type 2 diabetes, par- Early 18th Claude Bernard – hypothesised that glycogen was stored ticularly those over 50 years of age.7 century AD by the liver and secreted as a sugary substance into the blood. Overproduction of glucose was considered to be Charcot’s joint (neuropathic the cause of diabetes arthropathy) The feet of individuals with diabetes 1889 AD Joseph von Mering and Oscar Minkowski – discovered that mellitus can be afflicted with various the removal of a pancreas from a dog led to diabetes pathological conditions secondary to peripheral vascular disease, and/or 1893 AD Gustave-Edouard Laguesse – suggested that pancreatic . Poor manage- islet cells were involved in diabetes, and named them the ment of diabetes can lead to Islets of Langerhans peripheral neuropathy, resulting in sympathetic nerve damage and 1894 AD Moses Barron – linked damaged Islets of Langerhans to sensory loss in the foot. Neuropathic the cause of diabetes, and surmised that the substance foot ulcers may develop causing from these cells was the treatment for diabetes ischaemic mainly involving the distal metatarsals and proximal 1910 AD Edward Albert Sharpey-Schafer and Jean de Meyer – phalanges.16 Remodelling of the named the substance metatarsals and phalanges often changes the distal ends so that 1923 AD Frederick Banting and John Macleod – win Nobel Prize for the they form a distinctive tapered end discovery of insulin and production of insulin injections (also called diabetic osteopathy), often described as ‘pencil-shaped’.17 1936 AD Harold Percival Himsworth – makes the distinction Charcot’s joint, or a neuropathic joint, between type 1 and type 2 diabetes may also result and can lead to pro- gressive changes, such as fracture, 1977 AD Herbert Boyer genetically engineered synthetic human insulin osteolysis, fragmentation, new bone formation, subluxation, and, finally, for osteoarthritis.9 Osteoarthritis is Osteopaenia/osteoporosis complete joint disorganisation.8 more likely associated with obesity, Significant bone loss in both the which is a risk factor for type 2 dia- axial and appendicular skeleton has Osteoarthritis betes. Individuals with both type 2 been identified in individuals with Although osteoarthritis has been diabetes and obesity show an , although results are associated with type 2 diabetes, increase in both small and large contradictory regarding type 2 dia- diabetes itself is not a risk factor joint osteoarthritis.9 betes with some studies reporting

Pract Diab Int October 2010 Vol. 27 No. 8 Copyright © 2010 John Wiley & Sons 359 ORIGINAL ARTICLE Pathological skeletal remains from ancient Egypt: the earliest case of diabetes mellitus?

Figure 1. Location of Dayr al-Barsha in Egypt. Inset shows archaeological noted complication of unmanaged site divided into excavation zones, with Zone 9A circled diabetes, may affect gingival collagen turnover and osteoclast/osteoblast cellular function, resulting in osteopaenia and decreasing the abil- ity to maintain and remodel alveolar bone.12,22 Imbalances in lipid metab- olism, altered collagen metabolism, neutrophil dysfunction, and altered monocytic response are also associ- ated conditions that increase the like- lihood of diabetic individuals devel- oping periodontitis.12,19 Although all of the conditions listed previously may act in an additive fashion or work synergistically to affect the development of periodontal disease in the diabetic individual, it is clear that poor metabolic management and duration of the hyperglycaemic state are the two risk factors highly correlated with periodontitis. Poor metabolic control and ele- vated glucose levels can cause oral bacteria to multiply at an increased comparatively higher bone mass caries, periapical abscesses and ante- rate, leading to greater rates of density, particularly in those with mortem tooth loss can be diagnosed caries.12,20 Root surface caries are associated DISH.10,18 Lower bone on skeletal remains. The most com- reported to be more prevalent than mass density places these individuals mon oral complication of diabetes is coronal caries in patients with type 2 at higher risk for fractures, particu- periodontal disease.12,20 Increased diabetes,11 likely due to higher levels larly of the femoral neck. serum and glycosylated of chronic and severe periodontal dis- Osteopaenia and osteoporosis can haemoglobin (HbA1c) levels in indi- ease. Gingival recession in association result from many of the symptoms of viduals who do not manage their with periodontal disease, vascular diabetes. Polyuria, disruption of the diabetes have been correlated with changes, changes in oral microflora, absorption of calcium by the lower the development of gingivitis.19,21 and abnormal collagen metabolism intestine, parathyroid secretion When uncontrolled, gingivitis can are all associated with increased root problems, and alteration of vitamin progress into periodontal disease ulti- caries in diabetic patients.11 D regulation impact on the individ- mately resulting in alveolar bone loss. Periapical abscesses are also a ual’s ability to build and remodel Although the literature is unclear as recognised oral complication of dia- bone.10 Because type 1 diabetes com- to whether a change in microflora betes mellitus and result from bacteria mences at a young age, individuals contributes to the increased inci- entering the tooth and migrating are at a disadvantage for building the dence and severity of periodontal dis- through the apical foramen into the bone stores they will need during ease, the oral environment created bone surrounding the root tip.23 adulthood, placing them at risk for by unmanaged diabetes appears Microbiological studies have identi- developing osteoporosis as adults. to indicate this possibility.12,19,20 fied a trend toward increased apical While those suffering from chronic Increased levels of serum calcium in symptoms that may be related to the type 2 diabetes may experience bone saliva, resulting in calculus, as well as presence of more virulent micro- loss due to the same symptoms, they increased glucose levels in gingival organisms in necrotic pulp of those start bone loss later in life, and there- crevicular fluid and urea concentra- with diabetes, as, on average, the fore the loss may be less than in tions can promote an environment number of different microorganisms those afflicted with type 1 diabetes. that alters the oral microflora.12,19 detected is higher in diabetic vs Degenerative vascular changes affect- non-diabetic patients.24 Fusobacterium, Dental disease ing other parts of the body also affect Prevotella, Bacteroides, Peptostreptococcus, When uncontrolled, the oral compli- gingival tissues, interfering with the Porphyromonas, and Streptococcus are the cations of diabetes can be multiple delivery of nutrients and leukocytes predominant genera that have been and may include gingivitis and peri- and resulting in decreased oxygen isolated;24,25 however, chronic peri - odontitis, oral candidiasis, xerosto- and elimination of metabolic waste.19 apical infections in diabetes are more mia and salivary gland dysfunction, This condition may increase the frequently associated with specific caries, periapical abscesses, and ante- severity of periodontitis and also anaerobes, particularly Fusobacterium mortem tooth loss.12,19,20 Of these, affect the ability to heal wounds. nucleatum, Porphyromonas endodontalis periodontal disease, increased dental Non-enzymatic glycosylation, also a and Porphyromonas gingivalis.24,25

360 Pract Diab Int October 2010 Vol. 27 No. 8 Copyright © 2010 John Wiley & Sons ORIGINAL ARTICLE Pathological skeletal remains from ancient Egypt: the earliest case of diabetes mellitus?

Figure 2. Lateral view of scapulae showing comparative arthritic changes Figure 3. Diffuse idiopathic skeletal and development on the left glenoid cavity surface hyperostosis (DISH) showing fusion of thoracic vertebrae 6 through to 11 [left], and lumbar vertebrae 1 through to 3 [right]

Increased antemortem tooth loss brick tombs to shallow pit tombs with is a common problem in diabetic lesser quality funerary equipment. individuals. Multiple symptoms can All burials in this zone have been cause tooth loss, including increased dated to the late First Intermediate collagenase and hyperglycaemia. Period (ca. 2160–2055 BC) to early Individuals with diabetes may have Middle Kingdom (ca. 2055–1650 leaving the skeleton of the tomb an increase in the enzyme collage- BC), with some reuse during the owner almost complete and well nase, and when activated it may lead transition from the Second preserved.27,28 Given the position to the loss of connective tissue Intermediate Period (ca. 1650–1550 of the tomb in the cemetery and the attachment.12 Hyperglycaemia may BC) to the New Kingdom (ca. remains of the burial equipment, the also reduce the growth of fibroblast, 1550–1069 BC).26–29 burial in Tomb 10O22/1B Feature an element essential in building Tomb 10O22/1 consists of a rec- 277 tentatively dates between ca. collagen for the periodontium.12 tangular shaft (2.59m x 1.05m, 4.75m 2055 and 1911 BC.27–29 The loss of fibroblast growth and deep) at the bottom of which a burial The skeletal remains represent increased production of collagenase chamber (10O22/1B) opens to the an adult male, aged 40–45 years, affect the homeostasis of the peri- north.26,29 The entrance to the burial approximately 170cm in height. The odontal tissues, causing loose teeth chamber was blocked by a thin wall of individual’s pathological conditions and eventually tooth loss. Severe sun-dried clay bricks and coarse sand. are many, including: arthritic and periodontal disease, with or without Grave artifacts include metal model degenerative changes to the surface of periapical abscesses, can also destroy woodworking implements and the glenoid cavity of the left scapula alveolar bone and the alveolus, even- weapons, pieces of alabaster, the (Figure 2); fusion of the sixth through tually breaking down the periodon- rotted, dusty remains of the bottom to eleventh thoracic vertebrae and tal ligament and causing tooth loss. of a wooden coffin, some painted first through to third lumbar verte- The single-rooted anterior teeth are plaster remains of a burial mask, and brae (Figure 3); healed bilateral more likely to be affected first, as a small collection of ceramics. The metatarsophalangeal , they have less surface attachment to ceramic assemblage consists of sim- with fusions of the left medial alveolar bone than multi-rooted ple bowls, locally produced bottles, cuneiform and first metatarsal, and posterior teeth. plates and possibly some body shards the right third and fourth metatarsals of drop shaped jars, all dated to the (Figure 4). The bones of the foot are Findings and results early Middle Kingdom.26–29 In antiq- also very light, indicative of osteopae- The archaeological site of Dayr al- uity, looters had taken the ceramic nia/osteoporosis. In addition, this Barsha, Egypt, is located approxi- vessels out of the dark burial individual also displayed significant mately 270km south of Cairo on the chamber and smashed them in the asymmetrical brachydactyly of the east bank of the Nile (27° 45’ North; sunlight of the shaft to search for right metacarpals (Figure 5). 30° 54’ East) (Figure 1). The archae- any valuables they may have con- The individual also exhibits ological site is divided into 11 tained.27,28 A small offering consist- severe dental disease (Figure 6), research zones (Figure 1, inset). In ing of the four legs of a young calf including heavy wear, advanced peri- 2003 an individual with pathological was also recovered.27,28 Although the odontal disease, and significant cal- characteristics suggestive of diabetes burial in Tomb 10O22/1B Feature culus build-up on the lingual side of mellitus was excavated from Tomb 277 was looted during antiquity, phys- the mandibular and maxillary teeth. 10O22/1B Feature 277 in Zone 9A. ical evidence of a secondary burial There are also numerous mandibu- The tombs in this cemetery, within the shaft, dating to ca. 1550 lar dental caries, including the right arranged in walled complexes, range BC, suggests that the burial chamber distal surface of the first molar, the from large well-built vaulted mud had not been entered after that date, buccal side of the right third molar,

Pract Diab Int October 2010 Vol. 27 No. 8 Copyright © 2010 John Wiley & Sons 361 ORIGINAL ARTICLE Pathological skeletal remains from ancient Egypt: the earliest case of diabetes mellitus?

Figure 4. Bilateral metatarsophalangeal amputations, with fusion of the left the distal surface of the left first medial cuneiform and first metatarsal [arrow], and the right third and fourth molar, and the mesial and distal sur- metatarsals [right] face of the left second molar. All caries are located at the cemento- enamel junction (Figure 7). Maxillary antemortem tooth loss (Figure 8) includes the right and left first incisors, the left second incisor, the left first and second premolars, and the right and left second and third molars. Mandibular ante- mortem tooth loss includes the right and left second incisors, and the left first and second premolars.

Discussion When comparing the classic second- ary skeletal and dental effects of dia- betes mellitus with those found in the remains from Dayr al-Barsha, it is clear that this individual was most likely afflicted with diabetes mellitus. Although it cannot be diagnosed with certainty, the arthritic changes to the surface of the left glenoid cavity may have been the result of adhesive capsulitis. Interestingly, the Figure 5. Asymmetrical brachydactyly shown in the dorsal view of the right right scapula remained unaffected, hand [top, right], and side by side comparison of the right and left metacarpals showing unilateral affliction as is [bottom], shown from left to right, MC1, MC2, MC3, MC4 and MC5 common in diabetic individuals.6,14 Contiguous right side fusion of the sixth through to eleventh thoracic vertebrae and first through to third lumbar vertebrae is strongly sugges- tive of DISH.16 Even more telling is the condition of this individual’s feet (Figure 4). Bilateral amputations at the metatarsophalangeal and the tapering of the distal ends of the remaining metatarsals are indicative of diabetic foot complications. The particular healing pattern on the distal ends of the metatarsals (i.e. lat- eral-to-medial curvature) may result from foot wrapping or prosthetic use.30 Although advanced can cause similar bony responses in the feet,16 this individual does not display any other characteristics of leprosy. While the majority of the skeleton does not appear to be osteo- porotic, the foot bones are especially light with little cortical bone, indica- tive of osteopaenia, likely resulting from neuropathic arthropathy. One of the more curious pathologies is the asymmetrical brachydactyly of the right metacarpals. This condition appears to be either genetic or devel- opmental31 and most likely does not have a direct relationship with

362 Pract Diab Int October 2010 Vol. 27 No. 8 Copyright © 2010 John Wiley & Sons ORIGINAL ARTICLE Pathological skeletal remains from ancient Egypt: the earliest case of diabetes mellitus?

Figure 6. Skull of individual showing Figure 8. Maxillary [left] and mandibular [right] dentition showing advanced severe periodontal disease, dental wear, antemortem tooth loss, and pulp chamber exposure antemortem tooth loss, calculus formation, and apical abscesses

in both type 1 and type 2, but some The fact that this individual lived for are more frequently associated with a significant period of time with all one over the other. While adhesive of these pathological conditions capsulitis, DISH, and root caries are speaks of a society in which care for more prevalent in individuals who the sick and disabled was available, Figure 7. Examples of root caries on have type 2 diabetes, given the age at and also indicates that this individ- the mandibular right third molar [left] death and time period of this individ- ual may have had wealth and higher and left first molar [right] ual it is most likely that he suffered status allowing access to this level from type 2 diabetes. There is little of care. reported evidence in the anthropo- logical literature concerning ancient Acknowledgements skeletal diagnoses of diabetes melli- The authors would like to thank all tus. Those that do mention diabetes members of the Dayr al-Barsha as a potential diagnosis do so only expedition. Particular thanks go to in the presence of DISH, and point the Egyptian Supreme Council of to the likely association between Antiquities for continued support of obesity, DISH and diabetes.33,34 this expedition. This research was funded by the Katholieke Universiteit Conclusions Leuven and the Research Foundation, Diabetes mellitus is a disease prima- Flanders. diabetes mellitus; however, brachy- rily affecting soft tissue structures. dactyly and age of onset for type 2 Skeletal changes can appear in indi- Conflict of interest statement diabetes share regions of linkage on viduals who are chronic sufferers of There are no conflicts of interest. chromosome 12.31,32 diabetes mellitus, but these symp- Dental wear due to abrasion, cal- toms are secondary to the disease. References culus build-up, periapical abscesses There are no pathological skeletal References are available at www. and antemortem tooth loss are regu- characteristics exclusive to diabetes practicaldiabetesinternational.com. larly observed in this archaeological mellitus; therefore, a diagnosis of population; nevertheless, the extreme diabetes mellitus from skeletal Key points periodontal disease and root caries remains is very difficult. One indi- shown on this individual are unusual, vidual’s skeletal remains from the • Diagnosis of diabetes mellitus particularly for his age at death. Root archaeological site of Dayr al-Barsha, from skeletal remains is a difficult caries are observed in high frequen- present a myriad of pathological endeavour cies in individuals with uncontrolled characteristics that, when consid- • Skeletal remains from diabetes11 and are usually connected ered together, fit most of the second- Dayr al-Barsha, Egypt (dated to to severe periodontal disease and the ary skeletal symptoms expressed in ca. 2050–1911BC) provide exposure of the root surface. Severe chronic sufferers of type 2 diabetes. corroborative evidence for the periodontal disease has also led to the At present, the only way to trace this presence of type 2 diabetes antemortem loss of 12 teeth, which disease is through ancient written • This is the oldest and possibly the again is unusual for an individual of sources. This Middle Kingdom only conclusive skeletal evidence his age in this population. period skeleton, dated to 2050–1911 for diabetes mellitus in the Many of the secondary skeletal BC, may represent the earliest skele- archaeological record complications of diabetes are found tal evidence of diabetes mellitus.

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