Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e6
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Do altitude and climate affect paranasal sinus volume? Omer Tarık Selcuk a, *, Bekir Erol b, Levent Renda a, Ustun Osma a, Hulya Eyigor a, Behcet Gunsoy c, Buket Yagci b, Deniz Yılmaz a a
Antalya Research and Teaching Hospital, ENT Department, Varlik Mahallesi, Muratpasa, 07710 Antalya, Turkey Antalya Research and Teaching Hospital, Radiology Department, Varlik Mahallesi, Muratpasa, 07710 Antalya, Turkey c Gaziantep Dr Ersin Aslan State Hospital, ENT Depatment, Merkez, Gaziantep, Turkey b
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 12 March 2015 Accepted 19 May 2015 Available online xxx
Objective: The aim of this study was to evaluate the effect of climate and altitude differences on the volume of paranasal sinuses and on the frequency of anatomic variations by comparing the paranasal sinus tomograms (PNSCT) of patients who were born and living in a cold, dry climate at high altitude with those of patients who were born and living on the coast at sea level in a temperate climate. We also aimed to determine differences relating to gender. Material and methods: A total of 55 PNSCTs of 55 patients from the city center of Antalya and 60 PNSCTs of 60 patients from the city center of Agrı were evaluated and compared prospectively. The study included a total of 115 patients with a mean age of 44.75 ± 9.64 years (range, 27e63 years). Group 1 (Antalya) comprised 26 females (47.3%) and 29 males (52.7%) with a mean age of 36.7 ± 12.4 years. Group 2 (Agrı) comprised 25 females (41.7%) and 35 males (58.3%) with a mean age of 35.1 ± 13.4 years. Maxillary sinus volumes were 18.27 cm3 (range, 5.04e37.62) and 15.06 cm3 (4.11e41.40); sphenoid sinus volumes were 7.81 cm3 (1.80e20.63) and 6.35 cm3 (0.54e16.50); frontal sinus volumes were 5.51 cm3 (0.50e29.25) and 3.76 cm3 (0.68e22.81) respectively. Results: There was no statistically significant difference between the groups in term of volumes (p > 0.025). Both maxillary and frontal sinus volumes were greater in males compared to females (p < 0.025). The mean value of the maxillary sinus volume was 15.7 ± 5.3 cm3 and was significantly larger in males than in females (p ¼ 0.004). There was no statistically significant correlation between the volume of maxillary sinuses with age or side. There was no statistically significant difference between the groups in terms of septum deviation and concha bullosa rates (p ¼ 0.469 and p ¼ 0.388). Conclusion: There have been many studies of nasal cavity changes due to climatic conditions but this is the first study to measure the difference of paranasal sinus volumes. No difference was determined in the anatomic variations and volumes of the maxillary, frontal, sphenoid sinuses on PNSCT of patients from different climates and altitudes. © 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: Paranasal sinus Volume Climate Altitude Gender Concha bullosa
1. Introduction The mechanisms for paranasal sinus growth are not yet fully understood (Legent et al., 1991). The size of the sinus depends on the extent of pneumatization (Fatua et al., 2006) The development of the paranasal sinuses may differ according to age and between individuals, and sinuses may even demonstrate different development patterns on the two sides on an individual basis (Jun et al., 2005).
* Corresponding author. Tel.: þ90 5333254432; fax: þ90 2422494400. E-mail address: [email protected] (O.T. Selcuk).
The anatomy of the paranasal sinuses is highly complex, with many anatomic variations. Understanding this anatomy is very important to avoid complications during surgery. A detailed knowledge of anatomic variations in the paranasal sinus region is critical, especially for surgeons performing endoscopic sinus surgery. Variations or anomalies of the paranasal anatomic structures and mucosal abnormalities can be detected easily with coronal plane paranasal computed tomography (CT) imaging. Radiology also plays a major role in the preoperative evaluation (Kantarci et al., 2004). It has been suggested that nasal airflow and positive air pressure in the nasopharynx have an effect on the development of the paranasal sinuses and craniofacial skeleton (D'Ascanio et al.,
http://dx.doi.org/10.1016/j.jcms.2015.05.013 1010-5182/© 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Selcuk OT, et al., Do altitude and climate affect paranasal sinus volume?, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/j.jcms.2015.05.013
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O.T. Selcuk et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e6
2010; Kim et al., 2010). Nasal cavity shape is expected to show climatic adaptation (Noback et al., 2011). There have been many studies focusing on how the upper airway and the nasal region adapt to climate variations, and many have demonstrated climatedependent differences. However, to date, there have been no studies of the climatic and environmental effect on paranasal sinus volumes. The aim of this study was to evaluate the effect of the climate and altitude on the volume of the paranasal sinuses and on the frequency of anatomic variations by a comparison of PNSCTs of patients who were born and living in different climate conditions and at different altitudes. An additional aim was to determine differences relating to gender. 2. Materials and methods The study was performed at Agrı State Hospital, Otolaryngology Clinic and Antalya Research and Education Hospital, Otolaryngology and Radiology Clinics. Approval for the study was granted by the Agrı State Hospital Local Ethics Committee. Written informed consent was obtained from all the patients included in the study. The study included a total of 115 consecutive patients between the ages of 18 and 67 years with paranasal sinus CT between March 2010 and March 2012. The Antalya and Agrı groups comprised 55 and 60 patients respectively without sinonasal morbidity who were investigated for cephalgia etiology. Prospective evaluation was made of 55 paranasal sinus tomographies of 55 patients who were born and living in the city center of Antalya, which is on the Mediterranean coast at an altitude of 30 m. The climate is temperate with a mean annual temperature of 18.7 C (maximum 44.6 C; minimum 1.9 C) between 1954 and 2013. The second group comprised 60 paranasal sinus tomograms of 60 patients who were born and living in the city center of Agrı in the northeastern region of Turkey at an altitude of 1642 m in the mountain range that includes the highest peak of Anatolia, Mount Agrı (5137 m). The climate is cold and dry, with a mean annual temperature of 5.3 C (maximum 39.9 C, minimum 45.6 C) between 1954 and 2013. The PNSCT of the two groups were compared (www.dmi.gov.tr). On the paranasal scans, height, depth, and width were measured, and a cubital approximation of volume was determined
for each maxillary, frontal, and sphenoid sinus. The patients' coronal and axial CT images of the paranasal sinuses were obtained, and measurements were performed using the point where the diameter of the sinus was largest. For each patient, the right and left frontal and the right and left maxillary and sphenoid sinus volumes were separately calculated using the formula (axbxcx 0.52) (Figs. 1e3). Exclusion criteria were acute or chronic rhinosinusitis, previous nasal and/or paranasal surgery, impact septum deviation, antrochoanal polyp, nasal polyposis, history of maxillofacial trauma, benign or malignant tumors of the paranasal sinuses, recent upper respiratory tract infection, previous history of positive airway pressure treatment, and previous history of any systemic disease and systemic or/and topical drug use that could affect the paranasal sinuses and the nasal cavity. Patients who were born or lived in another city or county were also excluded. 3. Results The study included a total of 115 patients with a mean age of 44.75 ± 9.64 years (range, 27e63 years). Group 1 (Antalya) comprised 26 females (47.3%) and 29 males (52.7%) with a mean age of 36.7 ± 12.4 years. Group 2 (Agrı) comprised 25 females (41.7%) and 35 males (58.3%) with a mean age of 35.1 ± 13.4 years. The mean age and gender distribution of the patients living in Agrı and Antalya were statistically similar (p ¼ 0.511 and p ¼ 0.546) (Table 1). There was no statistically significant difference between the groups in terms of septum deviation and concha bullosa rates (p ¼ 0.469; and p ¼ 0.388) The incidence of sinus hypoplasia among patients living in Agrı and Antalya showed no statistically significant difference (p ¼ 1.000) (Table 2). Maxillary sinus volumes were 18.27 cm3 (range, 5.04e37.62) and 15.06 cm3 (4.11e41.40); sphenoid sinus volumes were 7.81 cm3 (1.80e20.63) and 6.35 cm3 (0.54e16.50); and frontal sinus volumes were 5.51 cm3 (0.50e29.25) and 3.76 cm3 (0.68e22.81). There was no statistically significant difference between the groups in term of volumes (p > 0.025). Both maxillary and frontal sinus volumes were greater in males compared to females (p < 0.025). The mean value of the maxillary sinus volume was 15.7 ± 5.3 cm3 and was significantly larger in males than in females (p ¼ 0.004). There was no
Fig. 1. Coronal and axial paranasal measurements made over the left frontal sinus computed tomographic scan.
Please cite this article in press as: Selcuk OT, et al., Do altitude and climate affect paranasal sinus volume?, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/j.jcms.2015.05.013
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Fig. 2. Coronal and axial measurements made over the right maxillary sinus paranasal computed tomographic scan.
Fig. 3. Coronal and axial computed tomographic scan of paranasal sinus made through measurements of the sphenoid sinus.
Table 1 Demographic characteristics according to region.
Age Gender Male Female
Agrı (n ¼ 60)
Antalya (n ¼ 55)
p Value
35.1 ± 13.4
36.7 ± 12.4
0.511 0.546
35 (58.3%) 25 (41.7%)
29 (52.7%) 26 (47.3%)
statistically significant correlation between the volume of maxillary sinuses with age or side. After exclusion of patients with hypoplasia, the median values of the calculated frontal sinus volume were similar in the two groups (p ¼ 0.985). No statistically significant differences were determined between the groups with respect to maxillary and sphenoid sinuses median volumes (p ¼ 0.153 and p ¼ 0.640).
The median values of frontal sinus volume calculated after the exclusion of hypoplastic patients based on Bonferroni adjustment were statistically similar between the Antalya and Agrı groups in both males and females (p ¼ 0.818 and 0.794). There were no statistically significant differences between the Antalya and Agrı group median values of maxillary sinus volume in both males and females according to the Bonferroni adjustment (p ¼ 0.207 and p ¼ 0.163). According to Bonferroni correction in terms of the median volumes of sphenoid sinus, there were no statistically significant differences between the Antalya and Agrı groups in either males or females (p ¼ 0.039 and p ¼ 0.193). After exclusion of patients with hypoplastic sinus, for patients living in Agrı, the median values of calculated frontal sinus volume were statistically significantly higher in males than in females (p ¼ 0.010). The median maxillary sinus volume was statistically significantly higher in males than in females (p ¼ 0.005). There was
Please cite this article in press as: Selcuk OT, et al., Do altitude and climate affect paranasal sinus volume?, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/j.jcms.2015.05.013
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O.T. Selcuk et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e6 Table 2 Paranasal sinus tomographic findings according to region.
Hypoplasia Frontal sinus volume Maxillary sinus volume Sphenoid sinus volume Septum deviation Concha bullosa
Agrı (n ¼ 60)
Antalya (n ¼ 55)
p Value
5 (8.3%) 3.76 ± 6.27 (0.68e22.81) 15.06 ± 8.22 (4.11e41.40) 6.35 ± 3.60 (0.54e16.50) 42 (70.0%) 22 (36.7%)
5 (9.1%) 5.51 ± 5.43 (0.50e29.25) 18.27 ± 7.82 (5.04e37.62) 7.81 ± 4.34 (1.80e20.63) 35 (63.6%) 16 (29.1%)
1.000 0.985 0.153 0.640 0.469 0.388
no statistically significant difference in the median sphenoid sinus volumes between males and females (p ¼ 0.605). After exclusion of patients with hypoplastic sinus, for patients living in Antalya, the median values of calculated frontal sinus volume were statistically significantly higher in males than in females (p ¼ 0.015). The median maxillary sinus volume was statistically significantly higher in males than in females (p ¼ 0.003). There was no statistically significant difference in median sphenoid sinus volumes between males and females (p ¼ 0.231) (Table 3). 4. Discussion As humans live in a wide range of environments, the nasal cavity has long been hypothesized to play a major role in climatic adaptation. No previous studies have focussed on the morphology of the nasal cavity behind the nasal aperture (Noback et al., 2011). In a cold climate, the nasal region adapts as a narrow nasal aperture, morphologically and functionally in increasing turbulence and thereby mixing the humidity of inspired air (Evteev et al., 2014). However, there is no previous study comparing paranasal volumes in different climates. In this study, we analyzed effects of altitude and climatic changes on the maxillary sinus volume, frontal sinus volume, and sphenoid sinus volume as well as the frequency of concha bullosa by examining the PNSCTs of patients living at different altitudes and in different climatic conditions. Previous studies have focused mainly on the differences of nasal cavity volume and outer nasal shape differences in different climates. Generally, dry and cold climates have been compared with hot and humid climates. In this study, a comparison was made of patients living in the cities of Agrı and Antalya. Maxillary sinus hypoplasia is an uncommon
Table 3 Frontal, maxillary, and sphenoid sinus volumes according to region and gender group. Agrı Frontal sinus volume Male 5.40 ± 7.13 (1.58e22.81) Female 3.09 ± 4.04 (0.68e18.13) b p Value 0.010 Maxillary sinus volume Male 19.25 ± 8.50 (6.00e41.40) Female 11.99 ± 6.50 (4.11e25.72) p Valueb 0.005 Sphenoid sinus volume Male 7.03 ± 3.95 (0.54e16.50) Female 6.00 ± 3.12 (1.20e13.13) b p Value 0.605
Antalya
p Valuea
6.20 ± 5.82 (0.84e29.25) 2.65 ± 4.32 (0.50e15.12) 0.015
0.818 0.794
22.14 ± 8.14 (5.04e37.62) 12.63 ± 5.84 (7.60e27.01) 0.003
0.207 0.163
9.00 ± 4.39 (2.10e20.63) 7.20 ± 3.93 (1.80e18.90) 0.231
0.039 0.193
a In comparison between the regions of Agrı and Antalya within gender groups, according to the Bonferroni adjustment, p < 0.025 for the results were considered statistically significant. b In comparisons between gender groups in the Agrı and Antalya regions in living subjects according to the Bonferroni adjustment, p < 0.025 for results was considered statistically significant.
condition (Stammberger, 1986). On coronal CT scans, Bolger et al. found the prevalence of unilateral hypoplastic maxillary sinus to be 10.4% (Bolger et al., 1990). In the current study, the prevalence of hypoplastic maxillary sinus was 0%, which may be due to the small number of patients. The incidence of frontal sinus hypoplasia among patients living in Agrı and Antalya showed no statistically significant difference (p ¼ 1.000). There was no statistically significant difference between the groups in terms of septum deviation and concha bullosa rates (p ¼ 0.469 and p ¼ 0.388). Orhan et al. determined the right and left maxillary sinus volumes to be 11.8 ± 4.7 cm3 and 11.5 ± 4.4 cm3, respectively, in a control group of 60 healthy individuals (Orhan et al., 2014). In the current study, the mean value of the maxillary sinus volume was found to be 15.7 ± 5.3 cm3 and was significantly larger in males than females (p ¼ 0.004). There was no statistically significant correlation between the volume of maxillary sinuses with age or side. These results were consistent with those of previous examinations (Ariji et al., 1994; Uchida et al., 1998). Gosau et al. reported female predominance in the smallvolume class (5e9 mL) (25% male, 75% female) when maxillary sinus volume was compared according to gender. In the middle volume classes (10e14 mL and 15e19 mL), a well-balanced gender distribution was determined (53.5% male, 46.5% female). Due to the small number of specimens, no statement could be made about the high volume class (20e24 mL). In the current study, a gender-related difference of maxillary sinus volume was noticed anecdotally, with males having a slightly larger volume than females, but the maxillary sinuses were not categorized in terms of dimensions. The study results of Gencer et al. suggest that maxillary sinus volumes tend to be higher on the contralateral side of severe septum deviations. In addition, the chance of finding maxillary sinusitis findings ipsilateral to severe septum deviation was significantly increased (Gencer et al., 2013). As severe septal deviations were excluded from the current study, it was not possible to compare sinus volume changes with severe septal deviations. In different studies, the volume of paranasal sinuses has been measured in different ways. In some anthropological studies, the volume has been measured by injecting various materials into the paranasal sinuses (Uchida et al., 1998; Schumacher et al., 1972). However, this type of procedure cannot be used on live subjects, and with injection methods, volume also has been underestimated in the presence of mucosal thickening and other sinus pathologies (Uchida et al., 1998; Schumacher et al., 1972; Pirner et al., 2009). The anatomical dimensions of the paranasal sinuses can be measured from CT images. In the current study, three-dimensional geometric morphometric methods and multivariate statistics were used to model and analyze the volume of the bony paranasal sinuses of two human population samples from two different climatic groups. Gosau et al. measured maxillary sinus volume, by water application through the semilunar hiatus in 65 cadavers, and the clinical implications of the findings were discussed. The medium maxillary sinus volume was found to be 12.5 mL (range, 5e22 mL) (Gosau
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et al., 2009). In the current study, the mean maxillary sinus volume was determined as 15.7 ± 5.3 cm3. The air-conditioning capacity of the nose is mainly dependent on the nasal temperature and the airflow caused by the airways and environmental changes. Nasal cavities have been categorized as tall and narrow or short and broad according to the morphological variation attributed to the ecogeographic adaptation to climate. People exposed to cold, dry environments present with tall and narrow features, and those who are exposed to hot humid environments present with short and broad features (Seren and Seren, 2009). The hypothesis of this study was that there could be a relationship between paranasal volumes and climate adaptation based on the above analyses; however, the results of this study demonstrated no difference. Keck et al. found relatively reduced nasal valve and turbinates in the hotehumid climate groups and increases in size in colder and drier climate populations (Keck et al., 2000). Their results showed that there is an anterior widening of the nasal cavity in hotehumid climate populations and that the anterior part of the nasal cavity is relatively narrow in cold and dry populations. A long and narrow respiratory passageway maximizes the mucosal surface area and air volume and this leads to a more turbulent airflow, facilitating the heat and moisture exchange that is a necessity in cold or dry environments (Seren and Seren, 2009). Corey et al. studied the nasal volume in different geographic groups and reported no significant differences (Corey et al., 1998). In a recent study, Yokley et al. found significant differences in the nasal cavity surface/volume ratio between different climates (Yokley, 2009). However, the relationship between climate and the paranasal sinus volumes has not been previously studied. Some recent studies have demonstrated that the maxilla is most closely correlated with climate among the cranial regions (Roseman, 2004; Harvati and Weaver, 2006; von Cramon-Taubadel, 2009; Smith, 2009). However, in the current study, no difference was found when considering paranasal volumes in a cold and dry climate and a temperate and humid climate, as in both groups, the median values were similar in the frontal sinus volume calculated after exclusion of patients with hypoplasia (p ¼ 0.985). The maxillary and sphenoid sinus median volumes showed no statistically significant differences between the groups (p ¼ 0.153 and p ¼ 0.640). The size of the sinus also depends on the extent of pneumatization (Fatua et al., 2006). One hypothesis about the function of paranasal sinuses is protection. Yu et al. reported that the volume of the frontal sinuses affected brain contusion and that larger frontal sinuses have a protective role for brain contusion resulting from head trauma (Yu et al., 2014). In the current study, frontal sinus volumes were found to be larger in males than in females, so it could be said that males are less likely than females to have have a brain contusion. In a study of globe ruptures, Kellman and Schmidt also reported that the paranasal sinuses protected the globe from rupture by allowing the orbital floor to fracture and to disperse the energy of the impact (Kellman and Schmidt, 2009). Greater maxillary and frontal sinus volumes were determined in males in the current study, which could protect males from globe ruptures. The major importance of this study is that it is the first study of the climatic and enviromental effect on paranasal sinus volumes. Additional study strengths were that it was prospective and blinded in design, and all patients were investigated clinically by the same otolaryngologist and radiologically by the same radiologist. There are also some limitations to the study. First, the number of patients was limited; second, there was no other control group living in another city; and finally, we did not classify the maxillary sinuses in terms of dimensions.
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5. Conclusion Numerous previous studies have focused on how the upper airway and the nasal region adapt to climate variations, and many have demonstrated climate-dependent differences. In the current study, the effects of altitude and climatic changes were evaluated on the maxillary sinus volume, frontal sinus volume, and sphenoid sinus volume and the frequency of anatomic variations by examining the PNSCTs of patients living at different altitudes and in different climatic conditions. However, no difference was found with respect to paranasal volumes in a cold and dry climate and in a temperate and humid climate. Further prospective studies with larger sample sizes are required. Funding There is no any sources of support in the form of grants. Conflict of interest There is no conflict of interest. References Ariji Y, Kuroki T, Moriguchi S, Ariji E, Kanda S: Age changes in the volume of the human maxillary sinus: a study using computed tomography. Dentomaxillofac Radiol 23: 163e168, 1994 Bolger WE, Woodruff Jr WW, Morehead J, Parsons DS: Maxillary sinus hypoplasia classification and description of associated uncinate process hypoplasia. Otolaryngol Head Neck Surg 103: 759e765, 1990 Corey JP, Gungor A, Nelson R, Liu XL, Fredberg J: Normative standards for nasal cross-sectional areas by race as measured by acoustic rhinometry. Otolaryngol Head Neck Surg 119: 389e393, 1998 D'Ascanio L, Lancione C, Pompa G, Rebuffini E, Mansi N, Manzini M: Craniofacial growth in children with nasal septum deviation: a cephalometric comparative study. Int J Pediatr Otorhinolaryngol 74: 1180e1183, 2010 Evteev A, Cardini AL, Morozova I, O'Higgins P: Extreme climate, rather than population history, explains mid-facial morphology of northern Asians. Am J Phys Antropology 153: 449e462, 2014 Fatua C, Puisorub M, Rotaruc M, Truta AM: Morphometric evaluation of the frontal sinus in relation to age. Trutad Ann Anat 188: 275e280, 2006 € Gencer ZK, Ozkiris M, Okur A, Karaçavus¸ S, Saydam L: The effect of nasal septal deviation on maxillary sinus volumes and development of maxillary sinusitis. Eur Arch Otorhinolaryngol 270: 3069e3073, 2013 Gosau M, Rink D, Driemel O, Draenert FG: Maxillary sinus anatomy: a cadaveric study with clinical implications. Anatomical Rec 292: 352e354, 2009 Harvati K, Weaver TD: Human cranial anatomy and the differential preservation of population history and climate signatures. Anat Rec A 288: 1225e1233, 2006 Jun BC, Song SW, Park CS, Lee DH, Cho KJ, Cho JH: The analysis of maxillary sinus aeration according to aging process; volume assessment by three-dimensional reconstruction by high resolutional CT scanning. Otolaryngol Head Neck Surg 132: 429e434, 2005 € Okur A, Karaman A: Remarkable Kantarci M, Karasen RM, Alper F, Onbas O, anatomic variations in paranasal sinus region and their clinical importance. Eur J Radiol 50: 296e302, 2004 Keck T, Leiacker R, Heinrich A, Kuhnemann S, Rettinger G: Humidity and temperature profile in the nasal cavity. Rhinology 38: 167e171, 2000 Kellman RM, Schmidt C: The paranasal sinuses as a protective crumple zone for the orbit. Laryngoscope 119: 1682e1690, 2009 Kim J, Song SW, Cho JH, Chang KH, Jun BC: Comparative study of the pneumatization of the mastoid aircells and paranasal sinuses using three-dimensional reconstruction of computed tomography scans. Surg Radiol Anat 32: 593e599, 2010 Legent F, Bordure P, Korb G, Calais C, Beauvillain C: Pneumosinus dilatans: longterm result of modelling osteoplasties. Ann Otolaryngol Chir Cervicofac 108: 30e33, 1991 Noback ML, Harvati K, Spoor F: Climate-Related variation of the human nasal cavity. Am J Phys Antropology 145: 599e614, 2011 Orhan I, Ormeci T, Aydin S, Altin G, Urger E, Soylu E, et al: Morrphometric analysis of the maxillary sinus in patients with nasal septum deviation. Eur Arch Otorhinolaryngol 271: 727e732, 2014 Pirner S, Tingelhoff K, Wagner I, Westphal R, Rilk M, Wahl FM, et al: CT-based manual segmentation and evaluation of paranasal sinuses. Eur Arch Otorhinolaryngol 266: 507e518, 2009 Roseman CC: Detecting interregionally diversifying natural selection on modern human cranial form by using matched molecular and morphometric data. Proc Natl Acad Sci USA 101: 12824e12829, 2004 Schumacher GH, Heyne HJ, Fanghanel R: Anatomy of the human paranasal sinuses. 2. Volumetric measurement. Anat Anz 130: 143e157, 1972
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Seren E, Seren S¸: Morphological adaptation of the nasal valve area to climate. Med Hypotheses 72: 471e472, 2009 Smith HF: Which cranial regions reflect molecular distances reliably in humans? evidence from three-dimensional morphology. Am J Hum Biol 21: 36e47, 2009 Stammberger H: Endoscopic sinus surgery-concepts in treatment of recurring rhinosinusitis. Part II. Surgical technique. Otolaryngol Head Neck Surg 94: 147e156, 1986 Uchida Y, Goto M, Katsuki T, Akiyoshi T: A cadaveric study of maxillary sinus size as an aid in bone grafting of the maxillary sinus floor. J Oral Maxillofac Surg 56: 1158e1163, 1998
von Cramon-Taubadel N: Revisiting the homoiology hypothesis: the impact of phenotypic plasticity on the reconstruction of human population history from craniometric data. J Hum Evol 57: 179e190, 2009 Yokley TR: Ecogeographic variation in human nasal passages. Am J Phys Anthropol 138: 11e22, 2009 Yu JL, Branstetter BF, Snyderman CH: Frontal sinus volume predicts incidence of brain contusion in patients with head trauma. J Trauma Acute Care Surg 76: 488e492, 2014
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Do altitude and climate affect paranasal sinus volume? Omer Tarık Selcuk a, *, Bekir Erol b, Levent Renda a, Ustun Osma a, Hulya Eyigor a, Behcet Gunsoy c, Buket Yagci b, Deniz Yılmaz a a
Antalya Research and Teaching Hospital, ENT Department, Varlik Mahallesi, Muratpasa, 07710 Antalya, Turkey Antalya Research and Teaching Hospital, Radiology Department, Varlik Mahallesi, Muratpasa, 07710 Antalya, Turkey c Gaziantep Dr Ersin Aslan State Hospital, ENT Depatment, Merkez, Gaziantep, Turkey b
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 12 March 2015 Accepted 19 May 2015 Available online xxx
Objective: The aim of this study was to evaluate the effect of climate and altitude differences on the volume of paranasal sinuses and on the frequency of anatomic variations by comparing the paranasal sinus tomograms (PNSCT) of patients who were born and living in a cold, dry climate at high altitude with those of patients who were born and living on the coast at sea level in a temperate climate. We also aimed to determine differences relating to gender. Material and methods: A total of 55 PNSCTs of 55 patients from the city center of Antalya and 60 PNSCTs of 60 patients from the city center of Agrı were evaluated and compared prospectively. The study included a total of 115 patients with a mean age of 44.75 ± 9.64 years (range, 27e63 years). Group 1 (Antalya) comprised 26 females (47.3%) and 29 males (52.7%) with a mean age of 36.7 ± 12.4 years. Group 2 (Agrı) comprised 25 females (41.7%) and 35 males (58.3%) with a mean age of 35.1 ± 13.4 years. Maxillary sinus volumes were 18.27 cm3 (range, 5.04e37.62) and 15.06 cm3 (4.11e41.40); sphenoid sinus volumes were 7.81 cm3 (1.80e20.63) and 6.35 cm3 (0.54e16.50); frontal sinus volumes were 5.51 cm3 (0.50e29.25) and 3.76 cm3 (0.68e22.81) respectively. Results: There was no statistically significant difference between the groups in term of volumes (p > 0.025). Both maxillary and frontal sinus volumes were greater in males compared to females (p < 0.025). The mean value of the maxillary sinus volume was 15.7 ± 5.3 cm3 and was significantly larger in males than in females (p ¼ 0.004). There was no statistically significant correlation between the volume of maxillary sinuses with age or side. There was no statistically significant difference between the groups in terms of septum deviation and concha bullosa rates (p ¼ 0.469 and p ¼ 0.388). Conclusion: There have been many studies of nasal cavity changes due to climatic conditions but this is the first study to measure the difference of paranasal sinus volumes. No difference was determined in the anatomic variations and volumes of the maxillary, frontal, sphenoid sinuses on PNSCT of patients from different climates and altitudes. © 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: Paranasal sinus Volume Climate Altitude Gender Concha bullosa
1. Introduction The mechanisms for paranasal sinus growth are not yet fully understood (Legent et al., 1991). The size of the sinus depends on the extent of pneumatization (Fatua et al., 2006) The development of the paranasal sinuses may differ according to age and between individuals, and sinuses may even demonstrate different development patterns on the two sides on an individual basis (Jun et al., 2005).
* Corresponding author. Tel.: þ90 5333254432; fax: þ90 2422494400. E-mail address: [email protected] (O.T. Selcuk).
The anatomy of the paranasal sinuses is highly complex, with many anatomic variations. Understanding this anatomy is very important to avoid complications during surgery. A detailed knowledge of anatomic variations in the paranasal sinus region is critical, especially for surgeons performing endoscopic sinus surgery. Variations or anomalies of the paranasal anatomic structures and mucosal abnormalities can be detected easily with coronal plane paranasal computed tomography (CT) imaging. Radiology also plays a major role in the preoperative evaluation (Kantarci et al., 2004). It has been suggested that nasal airflow and positive air pressure in the nasopharynx have an effect on the development of the paranasal sinuses and craniofacial skeleton (D'Ascanio et al.,
http://dx.doi.org/10.1016/j.jcms.2015.05.013 1010-5182/© 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Selcuk OT, et al., Do altitude and climate affect paranasal sinus volume?, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/j.jcms.2015.05.013
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O.T. Selcuk et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e6
2010; Kim et al., 2010). Nasal cavity shape is expected to show climatic adaptation (Noback et al., 2011). There have been many studies focusing on how the upper airway and the nasal region adapt to climate variations, and many have demonstrated climatedependent differences. However, to date, there have been no studies of the climatic and environmental effect on paranasal sinus volumes. The aim of this study was to evaluate the effect of the climate and altitude on the volume of the paranasal sinuses and on the frequency of anatomic variations by a comparison of PNSCTs of patients who were born and living in different climate conditions and at different altitudes. An additional aim was to determine differences relating to gender. 2. Materials and methods The study was performed at Agrı State Hospital, Otolaryngology Clinic and Antalya Research and Education Hospital, Otolaryngology and Radiology Clinics. Approval for the study was granted by the Agrı State Hospital Local Ethics Committee. Written informed consent was obtained from all the patients included in the study. The study included a total of 115 consecutive patients between the ages of 18 and 67 years with paranasal sinus CT between March 2010 and March 2012. The Antalya and Agrı groups comprised 55 and 60 patients respectively without sinonasal morbidity who were investigated for cephalgia etiology. Prospective evaluation was made of 55 paranasal sinus tomographies of 55 patients who were born and living in the city center of Antalya, which is on the Mediterranean coast at an altitude of 30 m. The climate is temperate with a mean annual temperature of 18.7 C (maximum 44.6 C; minimum 1.9 C) between 1954 and 2013. The second group comprised 60 paranasal sinus tomograms of 60 patients who were born and living in the city center of Agrı in the northeastern region of Turkey at an altitude of 1642 m in the mountain range that includes the highest peak of Anatolia, Mount Agrı (5137 m). The climate is cold and dry, with a mean annual temperature of 5.3 C (maximum 39.9 C, minimum 45.6 C) between 1954 and 2013. The PNSCT of the two groups were compared (www.dmi.gov.tr). On the paranasal scans, height, depth, and width were measured, and a cubital approximation of volume was determined
for each maxillary, frontal, and sphenoid sinus. The patients' coronal and axial CT images of the paranasal sinuses were obtained, and measurements were performed using the point where the diameter of the sinus was largest. For each patient, the right and left frontal and the right and left maxillary and sphenoid sinus volumes were separately calculated using the formula (axbxcx 0.52) (Figs. 1e3). Exclusion criteria were acute or chronic rhinosinusitis, previous nasal and/or paranasal surgery, impact septum deviation, antrochoanal polyp, nasal polyposis, history of maxillofacial trauma, benign or malignant tumors of the paranasal sinuses, recent upper respiratory tract infection, previous history of positive airway pressure treatment, and previous history of any systemic disease and systemic or/and topical drug use that could affect the paranasal sinuses and the nasal cavity. Patients who were born or lived in another city or county were also excluded. 3. Results The study included a total of 115 patients with a mean age of 44.75 ± 9.64 years (range, 27e63 years). Group 1 (Antalya) comprised 26 females (47.3%) and 29 males (52.7%) with a mean age of 36.7 ± 12.4 years. Group 2 (Agrı) comprised 25 females (41.7%) and 35 males (58.3%) with a mean age of 35.1 ± 13.4 years. The mean age and gender distribution of the patients living in Agrı and Antalya were statistically similar (p ¼ 0.511 and p ¼ 0.546) (Table 1). There was no statistically significant difference between the groups in terms of septum deviation and concha bullosa rates (p ¼ 0.469; and p ¼ 0.388) The incidence of sinus hypoplasia among patients living in Agrı and Antalya showed no statistically significant difference (p ¼ 1.000) (Table 2). Maxillary sinus volumes were 18.27 cm3 (range, 5.04e37.62) and 15.06 cm3 (4.11e41.40); sphenoid sinus volumes were 7.81 cm3 (1.80e20.63) and 6.35 cm3 (0.54e16.50); and frontal sinus volumes were 5.51 cm3 (0.50e29.25) and 3.76 cm3 (0.68e22.81). There was no statistically significant difference between the groups in term of volumes (p > 0.025). Both maxillary and frontal sinus volumes were greater in males compared to females (p < 0.025). The mean value of the maxillary sinus volume was 15.7 ± 5.3 cm3 and was significantly larger in males than in females (p ¼ 0.004). There was no
Fig. 1. Coronal and axial paranasal measurements made over the left frontal sinus computed tomographic scan.
Please cite this article in press as: Selcuk OT, et al., Do altitude and climate affect paranasal sinus volume?, Journal of Cranio-Maxillo-Facial Surgery (2015), http://dx.doi.org/10.1016/j.jcms.2015.05.013
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Fig. 2. Coronal and axial measurements made over the right maxillary sinus paranasal computed tomographic scan.
Fig. 3. Coronal and axial computed tomographic scan of paranasal sinus made through measurements of the sphenoid sinus.
Table 1 Demographic characteristics according to region.
Age Gender Male Female
Agrı (n ¼ 60)
Antalya (n ¼ 55)
p Value
35.1 ± 13.4
36.7 ± 12.4
0.511 0.546
35 (58.3%) 25 (41.7%)
29 (52.7%) 26 (47.3%)
statistically significant correlation between the volume of maxillary sinuses with age or side. After exclusion of patients with hypoplasia, the median values of the calculated frontal sinus volume were similar in the two groups (p ¼ 0.985). No statistically significant differences were determined between the groups with respect to maxillary and sphenoid sinuses median volumes (p ¼ 0.153 and p ¼ 0.640).
The median values of frontal sinus volume calculated after the exclusion of hypoplastic patients based on Bonferroni adjustment were statistically similar between the Antalya and Agrı groups in both males and females (p ¼ 0.818 and 0.794). There were no statistically significant differences between the Antalya and Agrı group median values of maxillary sinus volume in both males and females according to the Bonferroni adjustment (p ¼ 0.207 and p ¼ 0.163). According to Bonferroni correction in terms of the median volumes of sphenoid sinus, there were no statistically significant differences between the Antalya and Agrı groups in either males or females (p ¼ 0.039 and p ¼ 0.193). After exclusion of patients with hypoplastic sinus, for patients living in Agrı, the median values of calculated frontal sinus volume were statistically significantly higher in males than in females (p ¼ 0.010). The median maxillary sinus volume was statistically significantly higher in males than in females (p ¼ 0.005). There was
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O.T. Selcuk et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2015) 1e6 Table 2 Paranasal sinus tomographic findings according to region.
Hypoplasia Frontal sinus volume Maxillary sinus volume Sphenoid sinus volume Septum deviation Concha bullosa
Agrı (n ¼ 60)
Antalya (n ¼ 55)
p Value
5 (8.3%) 3.76 ± 6.27 (0.68e22.81) 15.06 ± 8.22 (4.11e41.40) 6.35 ± 3.60 (0.54e16.50) 42 (70.0%) 22 (36.7%)
5 (9.1%) 5.51 ± 5.43 (0.50e29.25) 18.27 ± 7.82 (5.04e37.62) 7.81 ± 4.34 (1.80e20.63) 35 (63.6%) 16 (29.1%)
1.000 0.985 0.153 0.640 0.469 0.388
no statistically significant difference in the median sphenoid sinus volumes between males and females (p ¼ 0.605). After exclusion of patients with hypoplastic sinus, for patients living in Antalya, the median values of calculated frontal sinus volume were statistically significantly higher in males than in females (p ¼ 0.015). The median maxillary sinus volume was statistically significantly higher in males than in females (p ¼ 0.003). There was no statistically significant difference in median sphenoid sinus volumes between males and females (p ¼ 0.231) (Table 3). 4. Discussion As humans live in a wide range of environments, the nasal cavity has long been hypothesized to play a major role in climatic adaptation. No previous studies have focussed on the morphology of the nasal cavity behind the nasal aperture (Noback et al., 2011). In a cold climate, the nasal region adapts as a narrow nasal aperture, morphologically and functionally in increasing turbulence and thereby mixing the humidity of inspired air (Evteev et al., 2014). However, there is no previous study comparing paranasal volumes in different climates. In this study, we analyzed effects of altitude and climatic changes on the maxillary sinus volume, frontal sinus volume, and sphenoid sinus volume as well as the frequency of concha bullosa by examining the PNSCTs of patients living at different altitudes and in different climatic conditions. Previous studies have focused mainly on the differences of nasal cavity volume and outer nasal shape differences in different climates. Generally, dry and cold climates have been compared with hot and humid climates. In this study, a comparison was made of patients living in the cities of Agrı and Antalya. Maxillary sinus hypoplasia is an uncommon
Table 3 Frontal, maxillary, and sphenoid sinus volumes according to region and gender group. Agrı Frontal sinus volume Male 5.40 ± 7.13 (1.58e22.81) Female 3.09 ± 4.04 (0.68e18.13) b p Value 0.010 Maxillary sinus volume Male 19.25 ± 8.50 (6.00e41.40) Female 11.99 ± 6.50 (4.11e25.72) p Valueb 0.005 Sphenoid sinus volume Male 7.03 ± 3.95 (0.54e16.50) Female 6.00 ± 3.12 (1.20e13.13) b p Value 0.605
Antalya
p Valuea
6.20 ± 5.82 (0.84e29.25) 2.65 ± 4.32 (0.50e15.12) 0.015
0.818 0.794
22.14 ± 8.14 (5.04e37.62) 12.63 ± 5.84 (7.60e27.01) 0.003
0.207 0.163
9.00 ± 4.39 (2.10e20.63) 7.20 ± 3.93 (1.80e18.90) 0.231
0.039 0.193
a In comparison between the regions of Agrı and Antalya within gender groups, according to the Bonferroni adjustment, p < 0.025 for the results were considered statistically significant. b In comparisons between gender groups in the Agrı and Antalya regions in living subjects according to the Bonferroni adjustment, p < 0.025 for results was considered statistically significant.
condition (Stammberger, 1986). On coronal CT scans, Bolger et al. found the prevalence of unilateral hypoplastic maxillary sinus to be 10.4% (Bolger et al., 1990). In the current study, the prevalence of hypoplastic maxillary sinus was 0%, which may be due to the small number of patients. The incidence of frontal sinus hypoplasia among patients living in Agrı and Antalya showed no statistically significant difference (p ¼ 1.000). There was no statistically significant difference between the groups in terms of septum deviation and concha bullosa rates (p ¼ 0.469 and p ¼ 0.388). Orhan et al. determined the right and left maxillary sinus volumes to be 11.8 ± 4.7 cm3 and 11.5 ± 4.4 cm3, respectively, in a control group of 60 healthy individuals (Orhan et al., 2014). In the current study, the mean value of the maxillary sinus volume was found to be 15.7 ± 5.3 cm3 and was significantly larger in males than females (p ¼ 0.004). There was no statistically significant correlation between the volume of maxillary sinuses with age or side. These results were consistent with those of previous examinations (Ariji et al., 1994; Uchida et al., 1998). Gosau et al. reported female predominance in the smallvolume class (5e9 mL) (25% male, 75% female) when maxillary sinus volume was compared according to gender. In the middle volume classes (10e14 mL and 15e19 mL), a well-balanced gender distribution was determined (53.5% male, 46.5% female). Due to the small number of specimens, no statement could be made about the high volume class (20e24 mL). In the current study, a gender-related difference of maxillary sinus volume was noticed anecdotally, with males having a slightly larger volume than females, but the maxillary sinuses were not categorized in terms of dimensions. The study results of Gencer et al. suggest that maxillary sinus volumes tend to be higher on the contralateral side of severe septum deviations. In addition, the chance of finding maxillary sinusitis findings ipsilateral to severe septum deviation was significantly increased (Gencer et al., 2013). As severe septal deviations were excluded from the current study, it was not possible to compare sinus volume changes with severe septal deviations. In different studies, the volume of paranasal sinuses has been measured in different ways. In some anthropological studies, the volume has been measured by injecting various materials into the paranasal sinuses (Uchida et al., 1998; Schumacher et al., 1972). However, this type of procedure cannot be used on live subjects, and with injection methods, volume also has been underestimated in the presence of mucosal thickening and other sinus pathologies (Uchida et al., 1998; Schumacher et al., 1972; Pirner et al., 2009). The anatomical dimensions of the paranasal sinuses can be measured from CT images. In the current study, three-dimensional geometric morphometric methods and multivariate statistics were used to model and analyze the volume of the bony paranasal sinuses of two human population samples from two different climatic groups. Gosau et al. measured maxillary sinus volume, by water application through the semilunar hiatus in 65 cadavers, and the clinical implications of the findings were discussed. The medium maxillary sinus volume was found to be 12.5 mL (range, 5e22 mL) (Gosau
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et al., 2009). In the current study, the mean maxillary sinus volume was determined as 15.7 ± 5.3 cm3. The air-conditioning capacity of the nose is mainly dependent on the nasal temperature and the airflow caused by the airways and environmental changes. Nasal cavities have been categorized as tall and narrow or short and broad according to the morphological variation attributed to the ecogeographic adaptation to climate. People exposed to cold, dry environments present with tall and narrow features, and those who are exposed to hot humid environments present with short and broad features (Seren and Seren, 2009). The hypothesis of this study was that there could be a relationship between paranasal volumes and climate adaptation based on the above analyses; however, the results of this study demonstrated no difference. Keck et al. found relatively reduced nasal valve and turbinates in the hotehumid climate groups and increases in size in colder and drier climate populations (Keck et al., 2000). Their results showed that there is an anterior widening of the nasal cavity in hotehumid climate populations and that the anterior part of the nasal cavity is relatively narrow in cold and dry populations. A long and narrow respiratory passageway maximizes the mucosal surface area and air volume and this leads to a more turbulent airflow, facilitating the heat and moisture exchange that is a necessity in cold or dry environments (Seren and Seren, 2009). Corey et al. studied the nasal volume in different geographic groups and reported no significant differences (Corey et al., 1998). In a recent study, Yokley et al. found significant differences in the nasal cavity surface/volume ratio between different climates (Yokley, 2009). However, the relationship between climate and the paranasal sinus volumes has not been previously studied. Some recent studies have demonstrated that the maxilla is most closely correlated with climate among the cranial regions (Roseman, 2004; Harvati and Weaver, 2006; von Cramon-Taubadel, 2009; Smith, 2009). However, in the current study, no difference was found when considering paranasal volumes in a cold and dry climate and a temperate and humid climate, as in both groups, the median values were similar in the frontal sinus volume calculated after exclusion of patients with hypoplasia (p ¼ 0.985). The maxillary and sphenoid sinus median volumes showed no statistically significant differences between the groups (p ¼ 0.153 and p ¼ 0.640). The size of the sinus also depends on the extent of pneumatization (Fatua et al., 2006). One hypothesis about the function of paranasal sinuses is protection. Yu et al. reported that the volume of the frontal sinuses affected brain contusion and that larger frontal sinuses have a protective role for brain contusion resulting from head trauma (Yu et al., 2014). In the current study, frontal sinus volumes were found to be larger in males than in females, so it could be said that males are less likely than females to have have a brain contusion. In a study of globe ruptures, Kellman and Schmidt also reported that the paranasal sinuses protected the globe from rupture by allowing the orbital floor to fracture and to disperse the energy of the impact (Kellman and Schmidt, 2009). Greater maxillary and frontal sinus volumes were determined in males in the current study, which could protect males from globe ruptures. The major importance of this study is that it is the first study of the climatic and enviromental effect on paranasal sinus volumes. Additional study strengths were that it was prospective and blinded in design, and all patients were investigated clinically by the same otolaryngologist and radiologically by the same radiologist. There are also some limitations to the study. First, the number of patients was limited; second, there was no other control group living in another city; and finally, we did not classify the maxillary sinuses in terms of dimensions.
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5. Conclusion Numerous previous studies have focused on how the upper airway and the nasal region adapt to climate variations, and many have demonstrated climate-dependent differences. In the current study, the effects of altitude and climatic changes were evaluated on the maxillary sinus volume, frontal sinus volume, and sphenoid sinus volume and the frequency of anatomic variations by examining the PNSCTs of patients living at different altitudes and in different climatic conditions. However, no difference was found with respect to paranasal volumes in a cold and dry climate and in a temperate and humid climate. Further prospective studies with larger sample sizes are required. Funding There is no any sources of support in the form of grants. Conflict of interest There is no conflict of interest. References Ariji Y, Kuroki T, Moriguchi S, Ariji E, Kanda S: Age changes in the volume of the human maxillary sinus: a study using computed tomography. Dentomaxillofac Radiol 23: 163e168, 1994 Bolger WE, Woodruff Jr WW, Morehead J, Parsons DS: Maxillary sinus hypoplasia classification and description of associated uncinate process hypoplasia. Otolaryngol Head Neck Surg 103: 759e765, 1990 Corey JP, Gungor A, Nelson R, Liu XL, Fredberg J: Normative standards for nasal cross-sectional areas by race as measured by acoustic rhinometry. Otolaryngol Head Neck Surg 119: 389e393, 1998 D'Ascanio L, Lancione C, Pompa G, Rebuffini E, Mansi N, Manzini M: Craniofacial growth in children with nasal septum deviation: a cephalometric comparative study. Int J Pediatr Otorhinolaryngol 74: 1180e1183, 2010 Evteev A, Cardini AL, Morozova I, O'Higgins P: Extreme climate, rather than population history, explains mid-facial morphology of northern Asians. Am J Phys Antropology 153: 449e462, 2014 Fatua C, Puisorub M, Rotaruc M, Truta AM: Morphometric evaluation of the frontal sinus in relation to age. Trutad Ann Anat 188: 275e280, 2006 € Gencer ZK, Ozkiris M, Okur A, Karaçavus¸ S, Saydam L: The effect of nasal septal deviation on maxillary sinus volumes and development of maxillary sinusitis. Eur Arch Otorhinolaryngol 270: 3069e3073, 2013 Gosau M, Rink D, Driemel O, Draenert FG: Maxillary sinus anatomy: a cadaveric study with clinical implications. Anatomical Rec 292: 352e354, 2009 Harvati K, Weaver TD: Human cranial anatomy and the differential preservation of population history and climate signatures. Anat Rec A 288: 1225e1233, 2006 Jun BC, Song SW, Park CS, Lee DH, Cho KJ, Cho JH: The analysis of maxillary sinus aeration according to aging process; volume assessment by three-dimensional reconstruction by high resolutional CT scanning. Otolaryngol Head Neck Surg 132: 429e434, 2005 € Okur A, Karaman A: Remarkable Kantarci M, Karasen RM, Alper F, Onbas O, anatomic variations in paranasal sinus region and their clinical importance. Eur J Radiol 50: 296e302, 2004 Keck T, Leiacker R, Heinrich A, Kuhnemann S, Rettinger G: Humidity and temperature profile in the nasal cavity. Rhinology 38: 167e171, 2000 Kellman RM, Schmidt C: The paranasal sinuses as a protective crumple zone for the orbit. Laryngoscope 119: 1682e1690, 2009 Kim J, Song SW, Cho JH, Chang KH, Jun BC: Comparative study of the pneumatization of the mastoid aircells and paranasal sinuses using three-dimensional reconstruction of computed tomography scans. Surg Radiol Anat 32: 593e599, 2010 Legent F, Bordure P, Korb G, Calais C, Beauvillain C: Pneumosinus dilatans: longterm result of modelling osteoplasties. Ann Otolaryngol Chir Cervicofac 108: 30e33, 1991 Noback ML, Harvati K, Spoor F: Climate-Related variation of the human nasal cavity. Am J Phys Antropology 145: 599e614, 2011 Orhan I, Ormeci T, Aydin S, Altin G, Urger E, Soylu E, et al: Morrphometric analysis of the maxillary sinus in patients with nasal septum deviation. Eur Arch Otorhinolaryngol 271: 727e732, 2014 Pirner S, Tingelhoff K, Wagner I, Westphal R, Rilk M, Wahl FM, et al: CT-based manual segmentation and evaluation of paranasal sinuses. Eur Arch Otorhinolaryngol 266: 507e518, 2009 Roseman CC: Detecting interregionally diversifying natural selection on modern human cranial form by using matched molecular and morphometric data. Proc Natl Acad Sci USA 101: 12824e12829, 2004 Schumacher GH, Heyne HJ, Fanghanel R: Anatomy of the human paranasal sinuses. 2. Volumetric measurement. Anat Anz 130: 143e157, 1972
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