THE ANATOMICAL RECORD 298:1072–1084 (2015)

CT Examination of Nose and Paranasal Sinuses of Egyptian Mummies and Three Distinct Human Population Groups: Anthropological and Clinical Implications 1,2  SAMUEL MARQUEZ, * WILLIAM LAWSON,3 KENNETH MOWBRAY,4 BRADLEY N. DELMAN,5 AND JEFFREY T. LAITMAN3,6,7,8 1 Department of Cell Biology, SUNY Downstate Medical Center, Brooklyn, New York 2 Department of Otolaryngology, SUNY Downstate Medical Center, Brooklyn, New York 3 Department of Otolaryngology, Icahn School of Medicine at Mount Sinai, New York, New York 4 Division of Anthropology, American Museum of Natural History, New York, New York 5 Department of Radiology, Icahn School of Medicine at Mount Sinai, New York, New York 6 Center for Anatomy and Functional Morphology, Icahn School of Medicine at Mount Sinai, New York, New York 7 New York Consortium in Evolutionary Primatology (NYCEP), New York, New York 8 Department of Medical Education, Icahn School of Medicine at Mount Sinai, New York, New York

ABSTRACT The interaction of nasal morphology and climatic conditions has resulted in diverse hard- and soft-tissue configurations across human population groups. While the processes of skull pneumatization are not fully understood, the invasions of the paranasal sinuses [PNS] into the cranium have contributed to assorted morphologies. Human migratory patterns and the strong association with climatic variables through time and space may explain this diversity. This study examined four multiregional populations of which two are from Egypt but of widely divergent eras. Three Egyptian mummies [EG-M] from the middle kingdom were CT scanned providing a unique opportunity to investigate the status of PNS anatomy within a time frame from 1567 BCE to 600 CE and compare it to a contemporary Egyptian [EG] (n 5 12) population. Dry skulls of Inuit [IT] (n 5 10) and East African [EA] (n 5 8) provide out-group comparisons, as one group represents an isolated geographic environment far different from that of Egypt and the other group inhabiting distinct environmental conditions albeit located within the same continent. Results showed EG-M and EG frontal sinus volumes were diminutive in size with no statistically significant difference between them. Maxillary sinus size values of EG-M and EG clustered together while IT and EA significantly differed from each other (P 5 0.002). The multiregional groups exhibited population specific morphologies in their PNS anatomy. Ecogeographic localities revealed anatomical differences among IT and EA, while the potential time span of about 3,500 years produced only a negligible differ-

*Correspondence to: Samuel M arquez, Ph.D., Department of Cell Biology, SUNY Downstate Medical Center, 450 Clarkson Ave, Box 5, Brooklyn, NY 11203. E-mail: samuel.marquez@ downstate.edu C 2015 WILEY PERIODICALS, INC. V

Received 19 March 2014; Accepted 15 January 2015. DOI 10.1002/ar.23159 Published online in Wiley Online Library (wileyonlinelibrary. com).

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ence between the Egyptian groups. The small sample sizes incorporated into this research requires confirmation of the results by analyses of larger samples from each geographic region and with the integration of a larger group of Egyptian mummified remains. Anat Rec, 298:1072–1084, C 2015 Wiley Periodicals, Inc. 2015. V

Key words: nose; paranasal sinuses; frontal sinus; maxillary sinus; nasal complex; Egyptian Mummies; CT examination

The nose as a prominent organ of respiration and olfaction has had a complicated evolutionary history, which is reflected in the various functions performed by the modern human nasal complex (see Jankowski, 2011, 2013). The nasal complex (M arquez et al., 2014) acts directly in the transport and conditioning of respiratory airflow (imparting humidification and modification of temperature), olfaction, production of nitric oxide gas (in the paranasal sinuses), and presumably in the regulation of brain temperature via the pterygoid plexus of veins (i.e., Bosworth, 1888; Dean, 1988; Stockhorst and Pietrowski, 2004; Lundberg, 2008, respectively). The nose, aside from being the first line of defense for the entire respiratory system, serves as a critical region for adaptation to the wide spectrum of climatic factors (e.g., cold/dry, warm/ moist air) that impact on the survival of the species (e.g., Naftali et al., 2005; Harkema et al., 2006). Thomson and Buxton (1923) focused on the nasal index (the ratio of nasal width by nasal height 3 100) of human population groups at a global level, linking each group to climatic factors. Other studies of the external nose have shown that populations living in cold and dry climatic conditions have a more pronounced protrusion of the nose from the face, suggesting a physiological adaptation to the dry component of the air (Carey and Steegman, 1981). Anthropological and human biological studies also suggest that the adaptive significance of the nose may offer insight into the evolutionary forces that may have been in play for specific populations (Beall et al., 2012, M arquez et al., 2015). While human population studies investigating potential climatic effects on the external nasal region have focused on piriform aperture and nasal dimensions, such as nasal bridge elevation, elongation and protrusion (e.g., Carey and Steegman, 1981; Franciscus and Long, 1991), few have incorporated internal nasal cavity measures (but see Franciscus, 2003; Yokley, 2009; Nicholas and Franciscus, 2014), and fewer still have included paranasal sinus morphology (but see Rae et al., 2011; Holton et al., 2013). These are potentially significant omissions. The putative functions ascribed to the hollow spaces of the skull have been proposed over the last 2,000 years of recorded history (Blanton and Biggs, 1969; for historical reviews of proposed functional roles of paranasal sinuses see Witmer, 1997; Rae and Koppe, 2004; M arquez, 2008), but the biological role of the paranasal sinuses is still not well understood. Some of the functions proposed include humidifying and warming inspired air (O’Malley, 1924; Proetz, 1941; Gannon et al., 1997), secreting mucus to keep the nasal chambers moist (Eckert-Mobius, 1933;

Sato, 1938; Alger, 1943), and thermally insulating the nervous centers (Schaeffer, 1916; Dean, 1988; Koppe et al., 1999). However, most of these proposals have been criticized (see Braune and Clasen, 1877; Negus, 1954; Mekjavic et al., 2002, respectively). Recent studies have suggested that these sinuses may be tracking environmental conditions indicating respiratory adaptation (M arquez and Laitman, 2008). The analysis of paranasal sinus size in an adaptive context may be of clinical importance with respect to better understanding the pathogenesis of chronic sinusitis. Sinusitis is one of the most common health care complaints in this country, affecting more than 31 million people in the US in 1994, and studies shedding light on the causes of sinus variation would aid in implementing therapeutic strategies against this disease (Shankar et al., 1994). The advent of antibiotics has kept the disease from becoming a debilitating one, which in the past often led to death. The CT scanning of mummies offers a unique opportunity to examine the health status of sinonasal anatomy during the time period in which these mummies lived, particularly during the preantibiotic era. The second recent Egyptian group represents a population from a common geographic location in a time well after the age of antibiotics and other factors influenced by industrialization. Analyzing the two Egyptian populations will compare the size of the frontal and maxillary sinuses over a few thousand years in people living in a common geographical location with similar environmental conditions. Examination of the frontal and maxillary sinuses of two additional groups of recent human dry skull specimens, one also from the African continent and another from a different geographic region of the world, will permit outgroup comparison with the Egyptian subgroup populations but subject to different environmental conditions.

MATERIALS AND METHODS Mummified and skeletal material was obtained from the Von Luschan and osteological collections at the American Museum of Natural History (AMNH). The study sample comprised of two Egyptian mummy heads, an Egyptian dry skull that may have undergone the mortuary practice of mummification and adult human dry crania representing three different geographic human population groups. Adult status for all specimens was assessed by the appearance of fully erupted third molar maxillary dentition. The population groups including their sample size are as follows: 1) Egyptian mummy heads (n 5 2) and an Egyptian skull who may have undergone mummification (see below), 2) contemporary

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Fig. 1. A mummy head from Thebes, Egypt showing exceptional preservation in the cranial, orbital and nasal region. (Courtesy of the Division of Anthropology at the AMNH, cat. # VL/1248).

Egyptians within the last 150 years [n 5 2], 3) East Africa [n 5 8], and Alaskan Inuit [n 5 8]. The two mummy heads examined in this study were acquired by the AMNH in 1924 and are housed in the Felix von Luschan collection in the Division of Anthropology, AMNH. One head was separated from the body at the seventh cervical vertebral level at the time of their arrival at the AMNH (Fig. 1) but no vertebral elements was associated with the other mummy head (Fig. 2). Their catalog numbers are assigned as follows: VL/ 1248 and VL/1232 both from Thebes Egypt. According to Ms. Gisselle Garcia (Curatorial Collections Manager of the Division of Anthropology at the AMNH), the skull from El Hesa, Egypt (cat. # VL/3134 also from the Von Luschan collection) was probably at one point a mummy and then was subsequently defleshed along with many of the mummies from El Hesa donated to the AMNH by Von Luschan. The provenance of each of these skulls is fully documented as to their place of origin based on historical records of recovery. AMNH lacks chronologies for when these individuals lived. The two specimens from Thebes, Egypt provide morphological clues of post 17th Dynastical existence due to our documenting through CT scanning that the ethmoid regions are broken in these two skulls. Intentional damage to the ethmoid

Fig. 2. A mummy head from Thebes, Egypt with craniofacial soft tissue morphology preserved including auricle, orbital and labial regions. Note the external nasal region exhibits relatively little damage. The study of mummies thus presents an unprecedented opportunity to assess hard and soft tissue structures in ancient populations that are not possible via similarly aged dry cranial samples. (Courtesy of the Division of Anthropology at the AMNH, cat. # VL/1232).

regions indicates excerebration (the removal of cerebral tissue)—a practice that became commonplace in the New Kingdom but decreased during the Late Period. Cessation of excerebration came about toward the end of the 2nd Century CE and the practice of mummification ceased altogether with the Arab conquest in 600 CE. Combined features of ethmoid breakage and overall preservation of skulls provide a conservative chronological placement of these two mummies within 1567 BCE – 600 CE. Similarly, the estimated time of death for the El Hesa specimen together with the morphological evidence of a broken ethmoid region (Fig. 3) places the mummy in a chronological range from 1567 BCE – 600 CE, which covers a time frame from the 18 Dynasty through the latter end of Dynastical Egypt (Elliot Smith and WoodJones, 1910; David and Archbold, 2000; David, 2003). The second group represents present-day Egyptians (within the last 150 years) whose geographic locality are similar to that of the mummies. The third group of humans is from East Africa representing a hot and moist environment. The fourth group represents Ipiutak Inuits from present day Alaska. This archaeological sample is dated between 500 BCE to 500 CE representing pre-European contact, thus eliminating potential

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Fig. 3. A. Cranium from El Hesa, Egypt. Note the wide nasal aperture representing the purported “classic” platyrrhine configuration. B. Lateral view of the cranium showing prominent zygoma and mastoid process but no overtly prognathic features. C. Extensive damage to the ethmoid bone is viewed through the piriform aperture. A pencil was inserted through the foramen magnum, abutting against the clivus and emerging into view above the level of the posterior clinoid proc-

esses. The absence of the ethmoid bone permits the viewing of the pencil through the aperture. D. Basal view of the cranium. Note the dark coloration around the basiocciput where the mummy wrappings may have been removed, exposing the region to taphonomic processes (Courtesy of the Division of Anthropology at the AMNH, cat. # VL/3134).

confounding variables such as genetic admixture. The selection process of the crania was based on having intact foramina, fissures, and internal nasal morphologies. As sex assessment may be difficult to apply to the mummies, the recent dry skull material included a mixed sex sample to ensure a thorough treatment of comparative data analyses. All specimens were scanned with the same model scanner (i.e., GE HiSpeed Advantage CT scanner machine) in the Department of Radiology, Icahn School of Medicine at Mount Sinai. Mummy heads and the ElHesa skull were scanned in September of 1998 using 3 mm slice sections at 3-mm intervals. Images were pre-

sented with a “bone” algorithm to give the high-density bone the greatest edge representation. Coronal scans of 1.0 mm slice thickness were taken for all other dry skulls specimens. Use of the smallest thickness minimizes partial volume averaging, which affords the best possible spatial resolution perpendicular to the scan plane (see excellent reviews in R€ uhli and B€oni, 2000; Spoor et al., 2000; R€ uhli et al., 2004a). In CT reconstructions a major source of segmentation artifact is partial volume averaging. For example, when contrasting materials that occupy a voxel (a unit representing threedimensional space), the CT signal becomes a mixture of those materials. As bone and air both occupy a voxel, its

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CT signal may be below the range that is representative for bone. During scanning of crania this effect results in artificial low CT signal of thin bony structures. To minimize such digital data errors the slice thickness should be set at the smallest value the machine can allow. The minimum slice thickness that the GE scanner can scan at is 1.0 mm which was the preferred choice selected in this study. Display field of view (DFOV) pertains to the area covered by the image. Using DFOV parameters larger than the specimen would result in loss of resolution. All specimens were positioned in the supine position with some anchored by foam blocks, cloth tape and cotton sheets, while other specimens required only foam blocks. The position of the specimens will allow using the minimum DFOV parameters. Before actual scanning, scout beams ensure the position of the specimen to be aligned centered and perpendicular to the X-ray beam geometry. The CT digital intensity specifications (i.e., 120 kV and 250 mA) of the scanning machine was used on the mummy heads and mummy skull. Frontal and maxillary sinus volumes including endocranial volumes were derived from CT imaging or seed filling technique (see protocol in M arquez and Laitman, 2008). Volume calculations for paranasal sinuses were performed on a General Electric Advantage Windows 4 Workstation (GE Medical Systems, Milwaukee, WI). Briefly, the contour of each sinus was traced manually on each CT image the sinus was displayed on, yielding the cross-sectional area on each slice. All of these crosssectional areas (in mm2) for each sinus were summated and multiplied by the slice thickness (mm) to yield overall volume (mm3). Each sinus could further be designated by a certain color, allowing generation of threedimensional displays that show the contour of each sinus in a different color. Endocranial volume is a required measurement for size standardization among specimens. Quantitative sinus measures establish the range of variation of sinus diversity in Egypt and permits comparison between the differing climatic and environmental factors of North and East Africa and an Alaskan population, which may affect sinonasal morphology.

RESULTS Mummy head and neck VL/1248 shows absence of most of the external nose but the neck region is intact terminating at the seventh cervical vertebrae (Fig. 4). The damaged external nose allows a window into the nasal cavity showing a wide nasal aperture, a strongly expressed anterior nasal spine, intact inferior conchae and a deviated septum. Nasal bone angulation and the overall preservation of the lateral piriform aperture borders coupled with the markedly expressed anterior nasal spine permits an estimation of nasal projection comparable to a leptorrhine configuration with an obtuse nasofrontal angle value. Fiber optic examination confirms extensive damage in the ethmoid bony region. The bandage wrappings tightly follow the bony contours particularly in the areas of the frontal processes of the maxilla, zygoma, and in the frontal bone region (Fig. 5). In lateral view, the bandage wrappings have broken off in the parietal and occipital regions leaving a distinctive color pattern on the skull (Fig. 4a), which is similar to the coloration observed in the El-Hesa skull (Fig. 1 and see discussion below). The nasofrontal angle shows an

Fig. 4. a. The head of mummy VL/1248 is shown in lateral view with a portion of the neck still intact, terminating at the seventh cervical region. (Courtesy of the Division of Anthropology at the AMNH) b. Three-dimensional CT reconstruction of the same mummy reveals laryngeal apparatus and cranial sutures.

obtuse angle consistent with a platyrrhine nasal configuration. The lateral edge of the alar region is sufficiently preserved to assess the width of the nasal aperture, which closely matches the intercanthal distance (see Fig. 5).

CT EXAMINATION OF NOSE AND PARANASAL SINUSES

Fig. 5. A frontally oriented, close-up photograph of mummy VL/1248 demonstrating the application of bandage wrappings. Mesh cloth is visible over the frontal and nasal region. It follows the contours of the frontal processes of the maxilla. (Courtesy of the Division of Anthropology at the AMNH).

Fig. 6. An axial CT scan of mummy VL/1248 showing symmetrical maxillary sinuses and extensive mastoid air cell morphology.

Head and neck CT evaluation of individual VL/1248 showed a generalized absence of soft tissues. However, the skin contour parallels the structure of the underlying remaining bony structures. The mummified remains include head, mandible and neck. Accordingly, the assessments of each anatomical region are subdivided

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Fig. 7. An axial CT scan of individual in Fig. 6 showing frontal sinus (FS) morphology where the right FS predominates over the left.

accordingly below. Head: The head shows the mastoid air cells to be well formed bilaterally (Fig. 6). Middle and inferior turbinates are present. There is good formation of the maxillary, ethmoid, sphenoid (Fig. 6), and frontal sinuses (Fig. 7). The sphenoid sinuses have pneumatized into the pterygoid recesses, which is greater on the left side. There is disruption of the anterior ethmoid wall bilaterally, with the defects extending through the cribriform plates. Intracranially, the dura is retracted and no longer contacts the inner table. The tentorium cerebellum and falx cerebri are both present, but displaced from their anatomic positions. Most of the intracranial compartment is filled with air. A small volume of what presumably is brain is noted posteriorly, greater on left than right posterior cranial fossa. Pharynx: There is a shrunken tongue, a well-formed epiglottis, frenulum, and resulting paired valleculae. Larynx: There is good visualization of the aryepiglottic folds, the piriform fossa, the cricoid cartilage and possibly the arytenoids. The thyroid cartilage is visualized and appears symmetric. Maxilla and Mandible: The mandibular arch is intact. There is no significant degenerative change around the condylar heads. The maxillary third molars appear to have descended. The mandibular molars are somewhat angled, and their eruption cannot be reliably characterized. Loss of bone is noted around the tooth sockets of several teeth, including the right maxillary central incisor (#9), the right maxillary first molar (#14) and the left maxillary premolar (#28). Cervical: All cervical vertebra are present but portions of C-7 have been damaged in removal (Fig. 8). A bifid spinous process of C5 is noted. Assessment of the spinal canal reveals absence of spinal cord, but dura is seen extending down to the lower border of C-6. Minor degenerative disc disease or and degenerative facet disease are present.

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Fig. 8. A series of CT scans of the cervical region of mummy VL/1248 allowing assessment of vertebral canal content and zygapophyseal joint morphology.

Mummy head VL/1232 showed remarkable preservation in the facial region, particularly in the orbits preserving eyelid anatomy and in the nasal area presenting with the entire external nose (Fig. 9). The right alar region of the nose is somewhat collapsed, the left external naris was complete showing an external narial shape that is larger in width than in length. In lateral profile, there is a strongly expressed dorsum (i.e., nasal hump), which is usually associated with a large volume of bone and cartilage. The nasofrontal angle is somewhat obtuse and while this is usually associated with a platyrrhine nasal condi-

tion, this individual exhibits nasal bridge elevation and elongation (Fig. 10). External ear morphology is conserved with the right showing greater preservation of the helix down to the lobule (Fig. 11). The cranial base region reveals prominent occipital condyles and a spherical shaped foramen magnum (Fig. 12). The choanae are clearly demarcated and an unusually long left styloid process is noted (Fig. 12). The bandage wrappings used in the mummification process show some decay as a crackling pattern is observed in the frontal bone region and in other areas the bandage wrappings are no longer present.

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Fig. 11. A lateral view of mummy VL/1232 demonstrating that the mortuary practice of mummification can preserve external nasal morphology, including nasal projection and its alar dimensions. The external ear is well preserved to a remarkable degree of real life likeness that includes the helix, antihelix, portions of the crura of the antihelix, the tragus and cavum conchae. Note the mesh-like pattern from the bandage wrapping along the zygoma and zygomatic arch. (Courtesy of the Division of Anthropology at the AMNH).

Fig. 9. Photograph of Thebean mummy VL/1232 showing external nasal morphology, eyelid anatomy and labial composition of the mouth. The bandage wrappings have hardened over time and have begun to crack in different areas over the skull. (Courtesy of the Division of Anthropology at the AMNH).

Fig. 10. A close-up lateral view photograph of Fig. 9 showing a prominent dorsal hump with midvault nasal depression. The depressed nasal process of the frontal bone exaggerates the prominence of the nasal hump. These deformities are strongly suggestive of trauma. (Courtesy of the Division of Anthropology at the AMNH).

CT evaluation of individual VL/1232 shows an absence of most of the ethmoid cells including an absence of the anterior nasal septum probably the result of the mortuary practice of the mummification process. The right maxillary sinus is smaller than the left, possibly with sclerotic margins around the sinus walls (Fig. 13). Frontal sinuses are diminutive presenting as multi-lobulated cavities located posterior to the superciliary arches in the frontal bone (Fig. 14). There is absence of the second maxillary molar on the left, the third left mandibular molar and the second right mandibular molar. No cervical vertebrae are included with this specimen. The El-Hesa skull VL/3134 exhibits a wide nasal aperture with a nasal sill and a markedly defined anterior nasal spine. The anterior face of the maxilla is hollowed out creating a concave appearance. The distinct color stain pattern of the bony surface is similar to mummy head VL/1248 (Fig. 1) in the areas where the bandage wrappings had broken off (Fig. 3). Little remains of the ethmoid bony region when viewed through the piriform aperture, which is the signature sign for excerebration (Fig. 3c). The dentition is heavily worn, especially the incisor teeth. There are numerous missing teeth including the right central and lateral maxillary incisors, portions of the right maxillary canine. Also, the right premolar and first molar are missing probably lost antemortem. No mandible is included with this specimen. The Egyptian mummies and the El Hesa skull exhibited diminutive frontal sinus size comparable to contemporary members of the Egyptian population. The Egyptian groups demonstrated no statistical significant differences in size between each other (P > 0.05) employing student t test (see Tables 1 and 2). All three of modern populations exhibited statistically significant differences in maxillary sinus size. The East African population had the largest average maxillary sinus while

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Fig. 12. a. Photograph of the cranial base of VL/1232 demonstrating the tight wrapping of the bandage coverings over the bony surface, protecting the hard tissue anatomy. b. A close-up inferior view of left temporal region showing a long and pronounced styloid process. (Courtesy of the Division of Anthropology at the AMNH).

the Alaskan Inuit and the Egyptian populations were comparable to each other. No statistically significant differences were detected between the Egyptian populations. One of the mummy skulls - El Hesa (VL 3124) presented with mild hyperostosis frontalis interna in which bilateral thickening of the endocranial surface limited to areas anterior to the coronal suture developed (R€ uhli et al., 2004b).

DISCUSSION

Fig. 13. An axial CT scan through the maxilla of mummy VL/1232 showing the outline tracings of the maxillary sinuses used in determining their total volume.

One unique aspect of examining mummies is the opportunity for the investigator to observe the external soft tissue anatomy of the individual. This is in contrast to the traditional examination and measurement of skeletal remains, with subsequent attempts made to reconstruct its integumentary configuration. Those reconstructions are conjectural and may be highly inaccurate. The mummification process provides the direct observation of the face and the relationship of the softtissue anatomy to the bony structures. The recording of obtuse nasofrontal angle values on the mummy heads usually indicate a platyrrhine nasal configuration (see Milgrim et al., 1996; El-Hadidy et al., 2007) but the preserved external nose of the mummies contradicts this supposed association of bony nasal morphology to nasal

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profile. This, in and of itself, is a remarkable finding given that the sub-Saharan population groups with obtuse nasofrontal angles almost invariably exhibit a platyrrhine configuration—short but wide nose. To reconcile this apparent paradox, a revisit to a study by C. Loring Brace and others who when examining the Nubian population found that one cannot “force” the sample into preset categories (e.g., Africans vs. Europeans) but rather should consider them for who they are, as Egyptians (Brace et al., 1993). Their study of the Predynastic population of Upper Egypt and the Late Dynastic population of Lower Egypt showed that they were more closely related to each other than to any other population, suggesting continuity. The study found that Egyptians as a whole showed ties with the European Neolithic, North African, modern European, and

Fig. 14. Axial CT scan slice through the frontal bone of mummy VL/ 1232 showing the outline tracing of the frontal sinus, which presents as several loculated cells. Areas can be determined and then multiplied by the slice thickness of the scan, thus generating a volumetric measure. For this scan, the four frontal sinus areas were multiplied by 3 mm slice thickness, yielding volumes of 68, 102, 93, and 111 mm3. A sum volume of 374 mm3 (0.374 mL) was obtained.

even Indian population, but not with sub-Saharan Africa populations (Brace et al., 1993). The Brace et al. (1993) study suggested that the Egyptians had been in place since the Pleistocene and have been largely unaffected by either invasions, or migrations, resulting in ancient Egyptians remaining as Egyptians to the present times. However, Hellenthal et al. (2014) showed that genetic admixture to be an almost universal force shaping human populations.

Anthropological Implications The nasal region. Biogeography is the study of the distribution of species and ecosystems in geographic space and time. Emanating from this discipline are the biographic “rules,” which are statements about biological traits in widely distributed homeothermic species that vary in relation to climatic effects (Beall et al., 2012). As modern humans migrated throughout the world, human biologists have hypothesized that adaptations could be expressed as clines or as correlations between climatic factors such as temperature and biological traits (Beall et al., 2012). While the Bergmann and Allen rules show the relationship of species size and limb length to climate (Ruff, 1991), there is also Thomson’s rule involving the human nose, which states that populations living in cold and dry climates tend to have longer and narrower noses, while shorter and wider noses are associated with warm and humid conditions (Beall et al., 2012). The Ancient Egyptians living in a tropical desert environment were exposed to hot and arid air conditions. As arid air has a reduced moisture carrying capacity, evolutionary forces may have shaped the external nasal configuration by elevating its bridge, elongating its length and protrusion to accommodate the humidification component of the air conditioning of inspiratory airflow. Physiologically, air conditioning of inspiratory airflow requires temperature modification to or near core body temperature and must provide 100% humidification for the proper exchange of gases to occur in the lower respiratory tract (e.g., Negus, 1952; see also Wolf et al., 2004). Thus, populations confronted with reduced moisture capacity of the air they breath from exposure to opposite extremes of the temperature gradient may develop anatomical traits necessary to impart humidification of the inspired air (Brace et al., 1993). Natural selection operates on the variability of its population members and will promote differing morphologies since “nature exerts a constant pressure on the population as a whole to become better adapted” (Tattersall,

TABLE 1. Morphometrics on mummy heads, El Hesa skull and two contemporary Egyptian skulls Origin

Cat. ID

Nasal ht

Nasal bth

Nasal index

Pros-opis

FSV

MSV

ECV

Mummy Mummy El Hesa skull Gizeh, skull Gizeh, skull

VL/1232 VL/1248 VL/3134 VL/1178 VL/1181

52.96 50.61 49.87 48.92 48.18

32.75 25.75 28.72 27.16 27.94

61.84 50.88 57.59 55.52 56.81

215 210 198 199 205

5.8 5.0 6.4 5.9 7.0

17.2 16.3 17.0 16.8 19.0

1125.26 1054.81 1198.42 1110.96 1249.78

bth 5 breath. ht 5 height. Pros-opis 5 prosthion to opisthocranion. FSV 5 frontal sinus volume (cc). MSV 5 maxillary sinus volume (cc). ECV 5endocranial volume (cc).

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TABLE 2. Morphometric data of two distinct human population groups Origin

Cat. ID

Nasal ht

Nasal bth

Nasal Index

Pros-opis

MSV

ECV

Alaska Alaska Alaska Alaska Alaska Alaska Alaska Alaska East Africa East Africa East Africa East Africa East Africa East Africa East Africa East Africa

99/4585 99/4586 99/4308 99/4646 99/2884 99/4658 99/6686 99/6690 VL/4718 VL/393 VL/4724 VL/409 VL/394 VL/396 VL/408 VL/3272

49.98 54.84 49.25 48.14 54.24 47.34 52.53 57.02 49.7 51.4 48.4 49.6 52.9 46.7 40.4 39.1

25.34 23.14 22.36 23.69 24.04 22.71 23.45 23.94 26.9 29.6 29.5 28.3 28.4 26.6 28.2 26.4

50.70 42.20 45.40 49.21 44.32 47.97 44.64 41.99 54.12 57.59 60.95 57.06 53.69 56.96 69.80 67.52

198 191.5 195 193 211 198.5 217.1 216 201 214 202 214 214 215 196 196

15.2 19.8 19.9 10.5 17.5 17.9 9.6 18.9 28 33 38 31 27 36 16 15

1280 1280 1330 1093 1266 1413 1310 1466 1085 1364 987 1191 1224 1148 1164 1086

ht 5 height. bth 5 breath. Pros-opis 5 prosthion to opisthocranion. MSV 5 maxillary sinus volume (cc). ECV 5endocranial volume (cc).

2010, p. 20). Modern human populations exhibit climatic signatures associated with their ecogeographic provenance, which likely evolved independently along distinctive adaptive pathways (Hubbe et al., 2009). As a result, prediction of morphological outcomes for specific climatic conditions may not be tenable. For example, cold-living populations from North America exhibit narrowing of the piriform aperture while Northern Europeans exhibit nasal projection in addition to tall, narrow piriform apertures (Hubbe et al., 2009). Finally, the common climatic element of “dry” air for our Egyptian sample (i.e., low humidity) may be the key driving force for nasal shape as other studies have suggested (e.g., Weiner, 1954 but see Yokley, 2009 for a consideration of internal nasal cavity dimensions for its adaptive significance). Future studies investigating climatic adaptation of populations should focus on the combination of variables (i.e., hot and dry vs. cold and dry) in order to detect the evolutionary signal influencing these morphological traits.

Paranasal sinuses. The results of this study demonstrate that the Egyptian mummy population exhibited diminutive frontal sinus size. The estimated elapsed time frame of 3,400 to 2,500 years (i.e., 1567 BCE 1 1865 CE and 600 CE 1 1865 CE, respectively) produced only negligible differences between the Egyptian mummies and the contemporary Egyptian groups. Frontal sinus development appears to be related to the location of the native population being studied. The significant differences in the size of the frontal sinuses among all geographical groups suggest that conditions specific to an area such as climate and temperature have a more profound effect on the adaptive changes over time than more modern factors such as antibiotics or pollution. Frontal sinus size variation has been attributed to age (Koertvelyessy, 1972), sex (Buckland-Wright, 1970), and biological affinity (Brothwell, et al., 1968). Possible pathological variations in size may be due to enlargement from thinning of the sinus walls due to age, chronic inflammatory conditions, trauma, tumors, or obstruc-

tions of the nasolacrimal duct (Schuller, 1943). One recent study using cranial radiographs suggested that differences in size and shape could be due to environmental conditions (Christensen, 2004). Another study researched sinus size within Canadian Inuit populations, Canadians, groups of American Inuit and Native Americans. The results found no difference in frontal sinus size within the Canadian Eskimo populations based on their specific Canadian location or sex; a slightly smaller size was present in the Canadian groups compared with similar groups of American Inuits (Hanson and Owsley, 1980). Our CT evaluation between the mummies and the more recent Egyptian individuals reveal secular trends in frontal and maxillary sinus morphology.

Clinical findings. The possible CT finding of sclerotic margins found in the maxillary sinus walls of individual VL/1232 suggests chronic disease. The pathophysiologic cascade of events culminating to the present finding is complex. First, nasal congestion obstructs the natural ostium of the maxillary sinus impeding proper ventilation and drainage. Mucus secretions become stagnant leading to mucosal thickening with cilia dysmotility and respiratory epithelial damage. The thick mucosa coupled with the lack of drainage creates an ideal culture medium for bacterial growth within an enclosed cavity. With chronicity there is reactive sclerosis of the sinus walls in an attempt to contain the infection. This may explain why sinus surgery probably originated during the time of the New Kingdom of ancient Egypt (see Tange, 1991). According to noted European otolaryngologist Heinz Stammberger, the Ancient Egyptians already had detailed knowledge of the existence of the paranasal sinuses as evidenced by the anatomy-related statements found in the papyrus of Ebers and other Egyptian tomb inscriptions, which date back to 1500 BCE (Stammberger, 1989). This is a reasonable conjecture given that Ancient Egyptians during the mortuary practice removed the brain through the

CT EXAMINATION OF NOSE AND PARANASAL SINUSES

nose without a defect in the face or skull, which speaks to their knowledge of the topographic relationship of the brain to the roof of the ethmoid and the cribriform plate (Stammberger, 1989). More mummified individuals are required to calculate the prevalence of chronic sinus disease in a given population. Another particular clinical feature of interest was the presence of hyperostosis frontalis interna (HFI) in El Hesa, which was also reported by Armelagos and Chrisman (1988) in a Nubian case and has been associated with human fossils (e.g., Sangiran 2, Gibraltar 1 and Shanidar 5—see Anton, 1997). The significance of this morphology is that it has been linked to steroids (e.g., R€ uhli et al., 2004b) with implications to diet and behavioral patterns (Ruhli and Henenberg, 2002). HFI is relatively common in modern humans, averaging approximately 12.4% in contemporary post-mortem European specimens. This frequency appears to represent a significant change over time, since the condition is almost never detected in historic populations from diverse origins, including Native Americans, Israeli Bedouins, and somewhat more recent Hungarians (Hershkovitz et al., 1999). That it is found more frequently in females (nearly 5:1 F:M ratio), and that the severity in most populations is age-dependent, suggests a possible hormonal basis although exact mechanism remains elusive (Raikos et al., 2011). A more thorough examination of mummies from El Hesa is required to determine the incidence of its occurrence.

CONCLUSION Our study suggests that environmental conditions may play a significant role in the evolution of the nose and paranasal sinuses in humans. If the age ranges for the mummies are valid, then a time span from either 1292 BCE or 1938 BCE showed no effects on frontal and maxillary sinus morphology compared with contemporary Egyptians with environmental conditions being held relatively constant. Examining the sinonasal region of human population groups in other geographic localities revealed morphological changes in sinus anatomy presumably responding to environmental conditions as it may be considered the independent variable. These results corroborate the finding of clinal variation of the maxillary sinus seen in macaques (Rae et al., 2003), in the frontal sinus seen in Inuits (Koertvelyessy, 1972) and in the maxillary sinus of Inuits (Shea, 1977). The selective evolutionary pressures seen with this study reveals the adaptive physiologic role the sinus spaces may play as confirmed by their global diversity (Laitman, 2008). The polyethnic diversity seen today in sinus anatomy demonstrates how plastic and adaptive this region has been in response to selective pressures. What may have maximized fitness centuries ago now may predispose current human populations to sinus diseases from new selective pressures in the form of pollution, viral agents and xenobiotic compounds from our industrialized world.

ACKNOWLEGEMENTS The authors thank the following people who granted permission to study the osteological collections at the American Museum of Natural History: Gisselle Garcia,

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Curatorial Collections Manager and Paul Beelitz, Director of Collections and Archives. The authors are also indebted to Ian Tattersall from the Division of Anthropology at the AMNH for granting permission to CT scan the mummy heads. Finally, special thanks to Dr. Brent Rogers, who as a medical student, assisted in the early stages of the project.

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