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New method for estimating the volume and volume fractions of the nasal structures in the goose (Anser anser domesticus) using computed tomography images a
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B. Onuk , M. Kabak , B. Sahin , N.G. Ince & M.B. Selcuk
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Department of Anatomy, Faculty of Veterinary Medicine , Ondokuz May s University , Samsun , Turkey b
Department of Anatomy , Medical School, Ondokuz May s University , Samsun , Turkey
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Department of Anatomy, Faculty of Veterinary Medicine , stanbul University , stanbul , Turkey
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Department of Radiology, Medical School , Ondokuz May s University , Samsun , Turkey Accepted author version posted online: 30 May 2013.Published online: 01 Aug 2013. To cite this article: B. Onuk , M. Kabak , B. Sahin , N.G. Ince & M.B. Selcuk (2013) New method for estimating the volume and volume fractions of the nasal structures in the goose (Anser anser domesticus) using computed tomography images, British Poultry Science, 54:4, 441-446, DOI: 10.1080/00071668.2013.806980 To link to this article: http://dx.doi.org/10.1080/00071668.2013.806980
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British Poultry Science, 2013 Vol. 54, No. 4, 441–446, http://dx.doi.org/10.1080/00071668.2013.806980
New method for estimating the volume and volume fractions of the nasal structures in the goose (Anser anser domesticus) using computed tomography images B. ONUK, M. KABAK, B. SAHIN1, N.G. INCE2
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M.B. SELCUK3
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Department of Anatomy, Faculty of Veterinary Medicine, Ondokuz Mayıs University, Samsun, Turkey, 1Department of Anatomy, Medical School, Ondokuz Mayıs University, Samsun, Turkey, 2Department of Anatomy, Faculty of Veterinary Medicine, İstanbul University, İstanbul, Turkey, and 3Department of Radiology, Medical School, Ondokuz Mayıs University, Samsun, Turkey
Abstract 1. The conchae within the nasal cavity of poultry are important for water and energy conservation, but have not been experimentally evaluated. The aim of the present study was to determine the accuracy of volume and volume fraction estimates of the conchae, nasal septum and nasal cavity. 2. The nasal cavities of 7 adult goose heads were scanned using computed tomography (CT), with images sampled randomly at a 1/5 sampling fraction. Physical sections were obtained from the same samples, using an electric saw that had an adjustable section range, and provided 14 to 15 sections with a thickness of 2.5 mm. The section surface areas of the nasal cavity, nasal septum and conchae were estimated using the Cavalieri principle. Results obtained using the CT and physical section images were compared. Volumes and volume fractions obtained from the physical sections were accepted as the gold standard and differences in the CT images were determined. 3. Multiplication of the data obtained on the CT images with the deviation percentage of the physical sections produced normalised values. No differences were observed between the gold standard data and the CT images. While it was possible to normalise the obtained data using the gold standard values, the raw data could also be used for comparative studies because the deviations from normal would be similar for all groups. 4. Our study showed that the nasal structures could be estimated in vivo using CT images.
INTRODUCTION The nasal cavity is formed by the palatine process of the maxilla, the caudal part of the premaxillar bone, the vomer and the palatine bone (Getty, 1975). The nasal cavity is divided by the nasal septum into right and left spaces (Cover, 1953; Nickel et al., 1977; King and McLelland, 1984; Ocal and Erden, 2002). The nasal septum has a septal sinus that opens into the nasal cavity (Nickel et al., 1977; King and McLelland, 1984) and infections of this structure with organisms such as avian influenza, Mycoplasma gallisepticum, Mycoplasma meleagridis and laryngotracheitis are frequently seen in
poultry (Calnek et al., 1991). Three conchae present processes to the nasal cavity by twisting along the internal surface of the lateral wall in each half of this cavity. The vestibular region is the cranial part of the nasal cavity and includes the rostral nasal concha. The respiratory region is the medial part which includes the medial nasal concha, while the olfactory region is the caudal part including the caudal nasal concha (Cover, 1953; Getty, 1975; King and McClelland, 1984; Dyce et al., 2002; O’Malley, 2005). In some poultry, a fourth septal concha is present in addition to these three (Ocal and Erden, 2002).
Correspondence to: Burcu Onuk, Department of Anatomy, Faculty of Veterinary Medicine, Ondokuz Mayıs University, Samsun 55139, Turkey. E-mail:
[email protected] Accepted for publication 1 April 2013.
© 2013 British Poultry Science Ltd
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Conchae in the nasal cavity increase the surface area, including that of the respiratory epithelium, and disperse the inhaled air (Ahishali et al., 2006). Unlike mammalian conchae, the conchae in the nasal cavities of poultry have an important role in water and energy conservation. The cranial part of the nasal cavity is colder than the caudal part, which reduces exhalation of humidity in the air by converting it into water during expiration. This water conservation is important. It allows migratory birds to fly for long periods without the need for water, and it is also important for desert-dwelling birds (Getty, 1975; Ocal and Erden, 2002). Stereological methods are frequently used to calculate organ volumes in many fields (Howard and Reed, 1998; Sahin et al., 2001; Odaci et al., 2003; Ince and Kahvecioğlu, 2010). Similarly, radiography, magnetic resonance (MR) imaging and computed tomography (CT) are commonly used to diagnose many diseases. However, evaluations performed during radiological tests can fluctuate depending on the experience of the physician, the shape and density of the structure and the reflection of the image on to the screen, so that these evaluations are reported as biased (Lang et al., 1998; Schinina et al., 2001). Studies have revealed that the volume of a three-dimensional structure may be calculated using the Cavalieri principle (Calmon and Roberts, 2000; Roberts et al., 2000). However, such estimates deviate from the real values (Howard and Reed, 1998). The anatomical and physiological structures of the nose have been studied predominantly in different mammals (Grutzenmacher et al., 2011). Geometrical measurements of the nasal cavity have also been performed via acoustic rhinometry and CT in humans (Gilain et al., 1997) and in guinea pigs and rats (Straszek and Pedersen, 2004). However, we were unable to find any reports on the measurement of the volume of the nasal cavity and volume fraction of the nasal conchae in other mammals or in poultry. Also, the true volumes of these regions in animals are not, to our knowledge, published in the literature. The aim of the present study was to determine the applicability of a new method for carrying out these measurements, in order to add to the existing anatomy literature and to present a mean value for researchers who work in this area in the future.
MATERIALS AND METHODS A total of 7 domestic goose (Anser anser domesticus) heads were fixed in 10% formalin solution. The nasal cavities were imaged in the transverse direction by CT scanning (Figure A). Images with a thickness of 0.5 mm and size of 512 × 512 DPI were obtained using a Toshiba Aquilion 16 CT device and recorded in DICOM format for
transfer to a CD. They were sampled randomly to obtain a 1/5 sampling fraction of the sections using ImageJ software (a program distributed freely by the National Institute of Health of the USA). An electric bandsaw (Dewalt DW876) with an adjustable section range was used to obtain physical sections from the same samples. A total of 14 to 15 serial sections per head with a thickness of 2.5 mm were cut and transferred to a digital environment using an HP Laser Jet (M1005 MFP) scanner (Figure B). Cut surface areas of the conchae and nasal spaces in CT images and physical sections were estimated using the grid plug-in tool of the ImageJ program. Point counting grids with a range of 0.6–2.0 mm for physical sections and 3–7 mm for CT images were randomly superimposed over the samples for this purpose (Figure C). The cut surface areas of the total nasal cavity were estimated using the planimetry tool of the software. For this purpose, the borders of the nasal cavity were drawn on all sections using the polygon selection tool of ImageJ and the total volume of the nasal cavity was estimated by multiplying the total section surface area by the section thickness (Figure D). The section surface areas of the conchae and nasal septum were estimated by counting the points hitting the structures of interest. The number of points, the area represented by each point and the section thickness were used to estimate the total volume of the structure investigated, based on the Cavalieri principle of stereological methods. The estimation formula for the total volume of the nasal space was obtained as follows: V = t × a/p × ΣP, where V is the volume, t is the section thickness, a/p is the area represented by each point in the point counting grid and ΣP is the total number of points hitting the surface area (Sahin et al., 2003). The volume of the total nasal cavity was found using the following formula: V = t × ΣA, where V is the volume, t is the section thickness and ΣA is the total section surface area (Bilgic et al., 2005). The volume of the nasal space was determined by subtracting the volumes of the concha and the nasal septum from the total volume of the nasal cavity. The volume fraction of the conchae and septum in the nasal cavity was calculated by applying the following formula: Volume fraction = (conchae or septum volume/nasal cavity volume) × 100. (1) The coefficient of error (CE), which evaluates the efficiency of the number of chosen sections and the point density of the grid, was calculated according to the method reported by Gundersen and Jensen (1987).
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Figure Computed tomography (CT) images and physical sections showing the nasal structures of the goose and techniques used to obtain volume data. (A): A CT section of the nasal cavity in transverse section. (B): A physical section of the nasal cavity in transverse section. (C): A point counting grid superimposed on a physical section. (D): Application of the manual planimetry to obtain sectional cut surface area of the region of interest. 150 × 150 mm (300 × 300 DPI).
Data obtained from CT and physical section images were evaluated for the data structure and GENMOD (Generalised Linear Modal) procedure was used compare the methods using SAS (2006). The GENMOD procedure was used in the data sets for total volume of the nasal cavity, conchae volume, space volume, conchae fraction using a normal distribution function. Fitting models in data sets for nasal septum volume and nasal septum fraction were done using a Poisson distribution and logit link function due to the data structure. For fitting models to the data sets, space parameters were held fixed and also algorithms converged to 10−6. The scale parameter was estimated by maximum likelihood. The best-fit model was selected by scaled deviance and log likelihood parameters.
RESULTS
sectioning techniques (physical and CT sectioning). The statistics for the total volume of the nasal cavity and for the volumes of conchae, nasal septa and nasal space obtained by both techniques are presented in Table 1. Statistics of the fractions that comprised the conchae, nasal septa and nasal space are presented in Table 2. No statistically significant differences were found between measurements made by physical section or by CT for the total volume of the nasal cavity, the concha volume, the nasal space volume or the Table 1.
Descriptive data for the volume (cm3) of structures located in the nasal cavity of the goose
Measurement Total volume of the nasal cavity Concha volume Space volume
The volume and volume fractions of the structures in the nasal cavity of the goose were estimated using the Cavalieri principle in order to compare the results obtained from two different
Nasal septum volume 1
Sections1 Mean Min Max PS CT PS CT PS CT PS CT
6.43 6.97 2.35 2.13 2.28 2.53 1.80 2.30
5.45 6.29 2.00 1.75 1.81 2.03 1.36 1.82
7.39 8.11 2.96 2.48 2.99 3.31 2.11 2.69
CT, the section taken from computed tomography; PS, physical section.
SE 0.24 0.27 0.12 0.10 0.15 0.15 0.11 0.13
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Table 2. Descriptive data for the volume fraction (%) of the structures located in the nasal cavity of the goose Measurement Concha fraction Space fraction Nasal septum fraction
Sections1
Mean
Min
Max
SE
PS CT PS CT PS CT
36.64 30.70 35.41 36.35 27.95 32.95
31.56 26.11 31.36 31.40 23.82 29.00
41.91 35.14 42.41 41.77 33.31 35.89
1.63 1.50 1.79 1.55 1.35 0.96
1
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CT, the section taken from computed tomography; PS, physical section.
nasal septum volume (P > 0.05). No significant differences were found for the nasal space fraction or for the nasal septum fraction measured by physical section or CT (P > 0.05), but a significant difference was determined (P < 0.05) for the concha fraction measured by physical section (37%) and by CT (31%). When the values obtained by physical sections were accepted as the gold standard, the deviations were 6.71 for the total volume of the nasal cavity, –11.1 for the concha volume, 8.97 for the nasal space volume, 19.7 for the nasal septum volume, 2.17 for the nasal space fraction, – 19.7 for the concha fraction and 14.6 for the nasal septum fraction.
DISCUSSION Differences are known to exist in the nose and surrounding structures between different animal species as in other organs, due to natural adaptation. For example, the beaks of water birds are elongated in order to facilitate their feeding (Demirsoy, 1992). Taxonomic discriminations in birds are performed based on the presence or absence of certain structures. Birds may be categorised into 4 taxonomic groups according to their skull configuration: palaeognath, schizognath, desmognath and aegithognath. Differences are also present in various organs according to each group (Demirsoy, 1992). Within this context, the sizes of the nasal cavity and conchae have not been quantitatively evaluated in birds. Prior to performing comparative studies, evaluation of the validity of the method proposed in this study is first required. Therefore, the reliability of the measurements of volume and volume fractions of the nasal cavity and its components as determined from CT images from the domestic goose, which belongs to the desmognath group, were investigated. The data from CT sectioning could be normalised using the deviation values obtained in this study. This requires multiplication of the values found by CT calculation and the deviation fraction of the related structure. These normal values could be used for the assessment of pathologies that are causing inflammation and swelling in
nasal mucosa, including the conchae, in infections with avian influenza, Mycoplasma gallisepticum, Mycoplasma meleagridis and laryngotracheitis (Calnek et al., 1991). In addition, the present method could be applied for clinical and diagnostic purposes for avian diseases. The volume fraction was calculated in addition to the volume estimation. The sizes of organs are a function of the body sizes of the individuals, which is affected by the body weights of the subjects in the group. Therefore, performing comparative studies solely using the volume or size of the organs between groups may not be valid. The problem increases if only the volume value is used for comparisons among species and the use of the volume fraction instead of a direct volume parameter is more appropriate for comparisons between animal species. A general fractional relationship exists between components of normal anatomical structures of every species. For example, the fraction of conchae to the whole nasal cavity in the goose may differ within certain values: the fraction varied from 32.6 – 41.9% in this study. Because it bypasses the inconveniences already specified, evaluation of the volume fraction for comparisons among species will allow comparative studies to be conducted. These types of comparative studies could improve the reliability of assessing the functions of these structures. In this context, we concluded that there could be anatomical differences in the conchae and nasal cavities, between birds flying at high altitude and for long periods, and domestic birds. The Cavalieri method has become a common approach for calculating volumes of normal and pathological formations in CT scans (Clatterbuck and Sipos, 1997; Odaci et al., 2003; Emirzeoglu et al., 2007; Kayipmaz et al., 2011). Studies conducted on this type of image have enabled the evaluation of living individuals. Therefore, the necessity of using physical sections has been removed. Nevertheless, scans created by imaging methods may differ from the actual structures due to the imaging tool used, the nature of the structure examined or its surrounding tissues. This situation has been described as a partial voluming effect in imaging methods. The partial voluming effect occurs when a less dense structure presents as a smaller projection because of the effect of dense tissues over less dense tissues (Soret et al., 2007; Sahin et al., 2008). Solving this problem requires gold standard studies, such as the one we present here. Once the volume values calculated using physical sections are accepted as the gold standard, the true values may be obtained by multiplying changes appearing in CT images with deviation coefficients established in these studies. Section thickness in imaging methods can also alter organ projections in images. To solve
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this problem in quantitative studies, either the same section thickness should be used or the differences in the thickness over the projection should be determined by examining the volume change due to section thickness. We used the same section thickness in all subjects in this study, which minimised any effect of section thickness on images. The CT imaging method is preferable, because imaging requires a shorter time for scanning compared with MR imaging. Also, it supplies more sharply circumscribed images of osseous and muscle tissues and of internal organs in particular. It is commonly used to examine the nasal cavity and surrounding structures in clinical practice (Sahin et al., 2008). We were unable to find any reports in the literature that quantitatively evaluated the volume and volume fraction of the nasal structures using both physical and CT sections and it is believed that the present study is the first in this area of research. A combination of CT images and stereological methods is useful for researcher purposes. Quantitative data may be obtained from daily images by this means and the application of stereological methods is straightforward. Furthermore, the method is not affected by the direction of the images or by the assessor (Odaci et al., 2003). Data in DICOM format obtained after CT images were analysed using ImageJ, a free program, and volume and volume fraction values were determined. The approach used in our study could allow acquisition of valuable quantitative data without occupying CT devices and invoking additional costs. When CT images are used, the deviation percentages from the actual values can be normalised, as shown by the data presented in this study. In this way, the researcher can interpret CT images and make accurate evaluations when taking the existence of deviation into account. The study also showed that the composition of the nasal structure can also be estimated in vivo in different animal groups using CT imaging. Consequently, data acquisition may be possible without the need to euthanise animals, allowing the use of more animals and thereby reducing statistical error. The method may be the gold standard for morphometric studies that consider differences appearing between data from physical sections and data from CT sections.
ACKNOWLEDGEMENTS The authors acknowledge Dr. Serhat Arslan, Ondokuz Mayıs University, Faculty of Veterinary Medicine, Department of Biometry, for statistical analysis of the data sets.
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