Article http://dx.doi.org/10.26855/jamc.2021.06.004

3D Computer Reconstruction of the Airway and the Vascular Systems of the Lung of the Domestic Fowl, Gallus gallus Variant domesticu


John N. Maina1,*, Yolanda Ramonisi1, Reatlegile Mashiteng1, Lolo Mokae1, Jeremy D. Woodward2

1Department of Zoology, University of Johannesburg, Auckland Park, Johannesburg 2006, South Africa.

2Division of Medical Biochemistry and Structural Biology, Structural Biology Research Unit, University of Cape Town, Observatory 7925, South Africa.

*Corresponding author: John N. Maina

Published: May 18,2021


The avian respiratory system (the lung-air sac system) is exceptionally structurally complex and functionally efficient. The capacity of powered (active) flight in birds is largely attributed to these features. Although it has been investigated for a longtime, important questions on the bioengineering of the avian respiratory system still remain unclear and controversial. Among these are basis of the airflow dynamics in the lung, the structure and topographic arrangement of the airway- and the vascular systems and the shapes and sizes of the terminal respiratory units. Here, in attempt to resolve some of the issues, the lung of the domestic fowl, Gallus gallus variant domesticus, was investigated by three-dimensional (3D) serial section computer reconstruction. The bronchial-(airway) and the vascular systems were reconstructed and their morphologies thoroughly assessed to determine their morphologies and spatial relationships. Movies of the reconstructions were prepared and rotated to view the structures from different perspectives. Furthermore, the different parts of the pulmonary vasculature were extracted and reinserted into the reconstructions to determine whether anastomoses existed. The most important findings were: three main branches (= rami) of the pulmonary artery deliver venous (deoxygenated) blood to various parts of the lung; three main branches of the pulmonary vein drain arterial (oxygenated) blood from the lung; the third costal sulcus forms the approximate boundary between the cranial- and the caudal blood supply- and drainage regions of the lung and; at least up to the level of the interparabronchial arteries and veins, no anastomoses (interconnections) were observed between the branches of the pulmonary artery and vein.


[1] Sergé, A., Bailly, A. L., Aurrand-Lions, M., Imhof, B. A., Irla, M. (2015). For 3D: Full organ reconstruction in 3D, an automatized tool for deciphering the complexity of lymphoid organs. J Immunol Methods, 2015, 424: 32-42.

[2] Darwin, C. (1859). On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: John Murry.

[3] Nachtigall, W. (1997). Exploring with the microscope: a book of discovery and learning. London: Sterling Publica-tions.

[4] Savile, B., Bracegirdle, B. (1998). Introduction to light microscopy. New York: Springer.

[5] Van Helden, A., Dupré, S., Rob, V. G., Zuidervaart, H. (eds). (2011). The origins of the telescope. Amsterdam: The Amsterdam University Press.

[6] His, W. (1880). Anatomie menschlicher Embryonen. Leipzig: Vogel. 

[7] Kastschenko, N. (1886). Methode zur genauen rekonstruktion kleinerer makroskopischer gegenstande. Arch Anat Physiologie Abteilung ,1886; 1: 388-394.

[8] Odhner, T. (1911). Zum naturlichen System der digenen Trematoden IV. Zool Anz, 1911; 38: 513-531.

[9] Ohta, Y., Millhouse, E. W. (1967). Glass plate reconstruction from serial sections used in the study of neonatal bi-liary atresia. In: Stereology (Elias H ed). Berlin: Springer; 1967: pp. 302-303.

[10] Ward, S., Thomson, N., White, J. G., Brenner S. (1975). Electron microscopical reconstruction of the anterior sen-sory anatomy of the nematode, Caenorhabditis elegans. J Comp Neuro, 1975; 160: 313-337. 

[11] Brenner, S. (2009). In the beginning was the worm. Genetics, 2009; 182: 413-415.

[12] Teutsch, H. F., Schuerfeld, D., Groezinger, E. (1999). Three-dimensional reconstruction of parenchymal units in the liver of the rat. Hepatology, 1999; 29: 494-505.

[13] Woodward, J. D., Maina, J. N. (2005). A 3D digital reconstruction of the components of the gas exchange tissue of the lung of the muscovy duck, Cairina moschata. J Anat, 2005; 206: 477-492.

[14] Woodward, J. D., Maina, J. N. (2008). Study of the structure of the air and blood capillaries of the gas exchange tissue of the avian lung by serial section three-dimensional reconstruction. J Microsc, 2008; 230: 84-93.

[15] Song, W. C., Hu, K. S., Kim, H. J., Koh, K. S. (2007). A study of the secretion mechanism of the sebaceous gland using three-dimensional reconstruction to examine the morphological relationship between the sebaceous gland and the arrector pili muscle in the follicular unit. British J Dermatol, 2007; 157: 325-330.

[16] Sun, K., Zhang, J., Chen, T., Chen, Z., Chen, Z., Li, Z., H., Hu, P. (2009). Three-dimensional reconstruction and visualization of the median nerve from serial tissue sections. Microsurgery, 2009; 29: 573-577.

[17] Penczek, P. A. (2010). Fundamentals of three-dimensional reconstruction from projections. Methods in Enzymol, 2010; 482: 1-33. 

[18] Wu, X., Yu, Z., Liu, N. (2012). Comparison of approaches for microscopic imaging of skin lymphatic vessels. Scanning, 2012; 34: 174-180.

[19] Onozato, M. L., Klepeis, V. E., Yagi, Y., Mino-Kenudson, M. (2012). A role of three-dimensional (3D)- recon-struction in the classification of lung adenocarcinoma. Anal Cell Pathol, 2012; 35: 79-84.

[20] Miranda, K., Girard-Dias, W., Attias, M., de Souza, W., Ramos, I. (2015). Three-dimensional reconstruction by electron microscopy in the life sciences: an introduction for cell and tissue biology. Mol Reprod Dev, 2015; 82: 530-547.

[21] Baghaie, A., Tafti, A. P., Owen, H. A., D’Souza, R. M., Yu, Z. (2017). Three-dimensional reconstruction of highly complex microscopic samples using scanning electron microscopy and optical flow estimation. PLoS One, 2017; 12(4): e0175078.

[22] Chozinski, T. J., Mao, C., Halpern, A. R., Pippin, J. W., Shankland, S. J., Alpers, C. E., Najafian, R., Vaughan, J. G. Volumetric, nanoscale optical imaging of mouse and human kidney via expansion microscopy. Sci Rep., 2018; 8:10396. (doi 10.1038/s41598-018-28694-2). 

[23] Kartasalo, K., Latonen, L., Vihinen, J., Visakorpi1, T., Nykter, M., Ruusuvuoril, P. (2018). Comparative analysis of tissue reconstruction algorithms for 3D histology. Bioinformatics, 2018; 34: 3013-3021.

[24] Oliveira, M., Duarte, S. B., Giacomini, G., Pereira, P. C. M., de Souza, L. R., Miranda, J. R. A., Pina, D. R. A lung image reconstruction from computed radiography images as a tool to tuberculosis treatment control. J Venom Animal Toxins Incl Trop Dis, 2019; 25: e144918. (doi.org/10.1590/1678-9199-jvatitd-a449-19)

[25] Zhou, J. (1991). Visualization of four dimensional space and its applications (PhD Thesis; Purdue University Tech-nical Report); Number 91-084:1991. 

[26] Lorenz, U. J., Zewail, A. Observing liquid flow in nanotubes by 4D electron microscopy. Science, 2014; 344: 1496-1500.

[27] Bissell, M. J. (2017). Goodbye flat biology—time for the 3rd and the 4th dimensions. J Cell Sci., 2017; 130: 3-5. 

[28] Turing, A. M. (1952). The chemical basis of morphogenesis. Philos Trans R Soc (Lond) B, 1952; 237: 37-72.

[29] French, R. (1988). Invention and evolution design in nature and engineering. Cambridge: Cambridge University Press; 1988. 

[30] Sung, W. (2018). Statistical physics of biological matter. Dordrecht: Springer. 

[31] Sharp, T. A., Merkel, M., Manning, M. L., Liu, A. J. (2019). Inferring statistical properties of 3D cell geometry from 2D slices. PLoS One, 2019; 14, e0209892. (doi.org/10.1371/journal.pone.0209892)

[32] Murakami, M. (2012). Signaling required for blood vessel maintenance: molecular basis and pathological manife-stations. Int J Vasc Med Article 2012. (doi:10.1155/2012/293641)

[33] Simons, M., Gordon, E., Claesson-Welsh L. (2016). Mechanisms and regulation of endothelial VEGF receptor sig-naling. Nature Rev Mol Cell Biol, 2016; 17(10). (doi: 10.1038/nrm.2016.87)  

[34] Lee, G. Y., Keny, P. A., Lee, E. H., Bissell, M. J. (2007). Three-dimensional culture models of normal and malignant breast epithelial cells. Nature Methods, 2007; 4: 359-365.

[35] Glauco, S. (2010). Three-dimensional tissue culture based on magnetic cell levitation. Nature Nanotech, 2010; 5: 291-296. 

[36] Baker, B. M., Chen, C. S. (2012). Deconstructing the third dimension—how 3D culture microenvironments alter cellular cues. J Cell Sci., 2012; 125: 3015-3024. 

[37] Edmondson, R., Broglie, J., Adcock, A., Yang, L. (2014). Three-dimensional cell culture systems and their applica-tions in drug discovery and cell-based biosensors. Assay Drug Dev Technol, 2014; 12: 207-218.

[38] Zanoni, M., Piccinini, F., Arienti, C., Zamagni, A., Santi, S., Polico, R., Bevilacqua, A., Tesei, A. (2016). 3D tumor spheroid models for in vitro therapeutic screening: a systematic approach to enhance the biological relevance of data obtained. Sci Rep, 2016; 6: 19103. (doi: 10.1038/srep19103)

[39] Powell, K. (2017). Adding depth to cell culture. Sci Technol Feature, 2017; 361; 6402.

[40] Ravi, M., Paramesh, V., Kaviya, S. R., Anuradha, E., Solomon, P. F. D. (2015). 3D cell culture systems: advantages and applications. J Cell Physiol, 2015; 230: 16-26.

[41] Cavo, M., Fato, M., Peñuela, L., Beltrame, F., Raiteri, R., Scaglione, S. (2016). Microenvironment complexity and matrix stiffness regulate breast cancer cell activity in a 3D in vitro model. Sci Rep, 2016; 6: 35367. (doi:10.1038/srep35367)

[42] Fang, Y., Eglen, R. (2017). Three-dimensional cell cultures in drug discovery and development. SLAS Discov: Ad-vancing Life Sci., 2017; 22: 456-472.

[43] Langhans, S. (2018). Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front Pharmacol, 2018; 22: 456-472.

[44] Haycock, J. W. (2011). 3D cell culture: a review of current approaches and techniques. Methods Molec Biol, 2011; 695: 1-15.

[45] Levinthal, C., Ware, R. (1972). Three-dimensional reconstruction from serial sections. Nature, 1972; 236: 207-209.

[46] Perkins, W. J., Green, R. J. (1982). Three-dimensional reconstruction of biological sections. J Biomed Engineer, 1982; 4: 37-43.

[47] Latamore, G. B. (1983). Creating 3-D models for medical research. Comput Graphics World, 1983; 5: 31-38.

[48] Mercer, R. R., Crapo, J. D. Structure of the gas exchange region of the lungs determined by three- dimensional re-constructions. In: Toxicology of the lung (Gardner DE, Crapo JD, Massaro EJ eds). New York; Raven Press: pp. 43-70.

[49] Xu, Y. H., Lahvis, G., Edwards, H., Pilot, H. C. (2004). Three-dimensional reconstruction from serial sections in PC-windows platform by using 3D_ viewer. Comput Methods Programs Biomed, 2004; 76: 143-154.

[50] Anderson, J. R., Wilcox, M. J., Wade, P. R., Barrett, S. F. (2003). Segmentation and 3D reconstruction of biological cells from serial slice images. Biomed Sci Instrument, 2003; 39: 117-122.

[51] Rosenhain, S., Magnuska, Z. A., Yamoah, G. G., Rawashdeh, W. A., Kiessling, F., Gremse, F. (2018). A preclinical micro-computed tomography database including 3D whole body organ segmentations. Sci Data 5 2018. (Article number 180294) 

[52] Vints, K., Vandael, D., Baatsen, P., Pavie, B., Vernaillen, F., Corthout, N., Rybakin, V., Munck, S., Gounko, N. V. Modernization of Golgi staining techniques for high-resolution, 3-dimensional imaging of individual neurons. Sci Rep., 2019; 9(1). (Article number 130) (doi 10.1038/s41598-018-373777-x)

[53] Herman, G. T. (2009). Fundamentals of computerized tomography: image reconstruction from projection, 2nd edition. Berlin; Springer.

[54] Diaspro, A. E. (ed.) (2001). Confocal and two-photon microscopy: foundations, applications and advances. Wiley; VCH): 2001.

[55] Handschuh, S., Schwaha, T., Metscher, B. D. (2010). Showing their true colors: a practical approach to volume rendering from serial sections. BMC Dev Biol, 2010; 10: 41. (doi 10.1186/1471-213X-10-41)

[56] Wang, C. W., Gosno, E. B., Li, Y. S. (2015). Fully automatic and robust 3D registration of serial-section microscopic images. Sci Rep, 2015; 5: 15051. (doi 10.1038/srep15051) 

[57] Wang, Y., Xu, R., Luo, G., Wu, J. (2015). Three-dimensional reconstruction of light microscopy image sections: present and future. Front Med., 2015; 9:30-45.

[58] Born, G. (1883). Die Plattenmodelliermethode. Arch Mikrosk Anat, 1883; 22: 584-599.

[59] Strasser, H. (1886). Ueber das Studium der Schnittserien und über die Hülfsmittel, welche die Reconstruction der zerlegten Form erleichtern. Zeitschrifft Wissen Mikrosk, 1886; 3: 179-195.

[60] Strasser, H. (1987). Ueber die Methoden der plastischen Rekonstruktion. Zeittschrift Wissen Mikrosk, 1987; 4: 168-208.

[61] Weninger, W. J., Mohun, T. (2002). Phenotyping transgenic embryos: a rapid 3-D screening method based on epi-scopic fluorescence image capturing. Nature Genetics, 2002; 30: 59-65.

[62] Ewald, A. J., McBride, H., Reddington, M., Fraser, S. E., Kerschmann, R. (2002). Surface imaging microscopy, an automated method for visualizing whole embryo samples in three dimensions at high resolution. Dev Dyn, 2002; 225: 369-375.

[63] Rosenthal, J., Mangal, V., Walker, D., Bennett, M., Mohun, T. J., Lo, C. W. (2004). Rapid high resolution three-dimensional reconstruction of embryos with episcopic fluorescence image capture. Birth Defects Res C Em-bryol Today, 2004; 72: 213-223.

[64] Keller, P. J., Schmidt, A. D., Wittbrodt, J., Stelzer, E. H. (2008). Reconstruction of zebrafish early embryonic de-velopment by scanned light sheet microscopy. Science, 2008; 322: 1065-1069.

[65] Tsuchiya, M., Yamada, S. (2014). High-resolution histological 3D-imaging: episcopic fluorescence image capture is widely applied for experimental animals. Congenit Anom (Kyoto), 2014; 54: 250-251.

[66] Takaishi, R., Aoyama, T., Zhang, X., Higuchi, S., Yamada, S., Takakuwa, T. (2014). Three-dimensional reconstruc-tion of rat knee joint using episcopic fluorescence image capture. Osteoarthtitis Cartilage, 2014; 22: 1401-1409. 

[67] Kong, W., Du, W., Liu, K., Liu, H., Zhao, Z., Pu, M., Wang, C., Luo, X. (2018). Surface imaging microscopy with turntable penetration depth as short as 20 nm by employing the hyperbolic metamaterials. J Materials Chem C., 2018; 6(7). (doi: 10.1039/C7TC04748G)

[68] Geyer, S. H., Weninger, W. J. (2019). High-resolution episcopic microscopy (HREM): looking back on 13 years of successful generation of digital volume data of organic material for 3D visualisation and 3D display. Appl Sci., 2019; 9: 3826. (doi:10.3390/app9183826)

[69] Braumann, U. D., Scherf, N., Einen, J., Horn, L. C., Wentzensen, N., Loeffler, M., Kuska, J. P. (2007). Large histo-logical serial sections for computational tissue volume reconstruction. Methods Inf Med., 2007; 46: 614-622.

[70] Roberts, N., Magee, D., Song, Y., Brabazon, K., Shires, M., Crellin, D., Orsi, N. M., Quirke, R., Quirke, R., Quirke, P., Treanor, D. (2012). Towards routine use of 3D histopathology as a research tool. Am J Pathol., 2012; 180: 1835-1842. 

[71] Liu, B., Gao, X. L., Yin, H. X., Luo, S. Q., Lu, J. (2007). A detailed 3D model of the guinea pig cochlea. Brain Struct Funct, 2007; 212: 223-230. 

[72] Deluzio, T. G. B., Seifu, D. G., Mequanint, K. (2011). 3D scaffolds in tissue engineering and regenerative medicine: beyond structural templates? Pharmaceut Biopro, 2011; 1: 267-281.

[73] Yu, Y., Moncal, K. K., Li, J., Peng, W., Rivero, I., Martin, J. A., Ozbolat, I. T. (2016). Three-dimensional bioprinting using self-assembling scalable scaffold-free tissue strands as a new biolink. Sci Rep, 2016; 6: 28714. (doi: 10.1038/srep28714)

[74] Jensen, G., Morrill, C., Huang, Y. (2018). 3D tissue engineering, an emerging technique for pharmaceutical research. Acta Pharmaceut. Sinica B, 2018; 8: 756-766.

[75] Duncker, H. R. (1971). The lung-air sac system of birds: a contribution to the functional anatomy of the respiratory apparatus. Ergeb Anat Entwicklungsgesch, 1971; 45: 1-171.

[76] Duncker, H. R. (1972). Structure of avian lungs. Respir Physiol, 1972; 14: 44-63.

[77] Duncker, H. R. (1974). Structure of avian respiratory tract. Respir Physiol, 1974; 22: 1-19.

[78] Scheid, P. (1979). Mechanisms of gas exchange in bird lungs. Rev Physiol Biochem Pharmacol, 1979; 86: 137-186.

[79] McLelland, J. (1989). Anatomy of the lungs and air sacs. In: Form and function in birds, vol. IV (King AS, McLelland J eds). London; Academic Press: 1989: pp. 221-279. 

[80] Powell, F. L., Hopkins, S. R. (2004). Comparative physiology of lung complexity: implications for gas exchange. News Physiol Sci., 2004; 19: 55-60.

[81] Maina, J. N. (2005). The lung air sac system of birds: development, structure, and function. Heidelberg; Springer.

[82] Maina, J. N. (2006). Development, structure and function of a novel respiratory organ, the lung-air sac system of birds: To go where no other vertebrate has gone. Biol Rev., 2006; 81: 545-579.

[83] Maina, J. N. (2017). Pivotal debates and controversies on the structure and function of the avian respiratory system: setting the record straight. Biol Rev., 2017; 92: 1475-1504.

[84] Harvey, E. P., Ben-Tal, A. (2015). Robust unidirectional airflow through avian lungs: new insights from a piecewise linear mathematical mode. PLoS Comput Biol, 2015; 12(2): e1004637. 

[85] Coitier, V. (1573). Anatomie avium. Externum et Internarum Praecipalium Humani Corporis Partium Tabulae atque Anatomicae Exercitationes Observationesque Varieae. Germany; Norimbergae: 1573; pp. 130-133. 

[86] Maina, J. N. (2011). Bioengineering aspects in the design of gas exchangers: comparative evolutionary, morphological, functional, and molecular perspectives. Heidelberg: Springer.

[87] Fedde, R. (1980). The structure and gas flow pattern in the avian lung. Poult Sci., 1980; 59: 2642-2653.

[88] Wang, N., Banzett, R. B., Nations, C. S., Jenkins, E. A. (1992). An aerodynamic valve in the avian primary bron-chus. J Exp Biol, 1992; 262: 441-445.

[89] Maina, J. N., Singh, P., Moss, E. A. (2009). Inspiratory aerodynamic valving occurs in the ostrich, Struthio camelus lung: computational fluid dynamics study under resting unsteady state inhalation. Respir Physiol Neurobiol, 2009; 169: 262-270.

[90] Maina, J. N. The Morphometry of the avian lung. In: Form and function in birds, vol. 4 (King AS, McLelland J eds). London; Academic Press: pp. 307-368.

[91] Maina, J. N., King, A. S., Settle, J. G. (1989). An allometric study of the pulmonary morphometric parameters in birds, with mammalian comparison. Philos Trans R Soc Lond B, 1989; 326: 1-57.

[92] Tucker, V. A. Energetics of natural avian flight. In: Avian energetics (Paynter RA ed). Cambridge (MA); Nuttal Ornithological Club: pp. 298-333. 

[93] Maina, J. N. (2000). What it takes to fly: the novel respiratory structural and functional adaptations in birds and bats. J Exp Biol, 2000; 203: 3045-3064.

[94] Altshuler, D. L., Dudley, R. (2006). The physiology and biomechanics of avian flight at high altitude. Integr Comp Biol, 2006; 46: 4-8.

[95] Scott, G. R. (2011). Elevated performance: the unique physiology of birds that fly at high altitudes. J Exp Biol, 2011; 214: 2455-2462.

[96] Scott, G. R., Dawson, N. J. (2017). Flying high: The unique physiology of birds that fly at high altitudes. In: The biology of the avian respiratory system: evolution, development, structure and function (Maina JN ed). Heidelberg; Springer; 2017: pp. 113-128.

[97] Laguë, S. L. (2017). High altitude champions: birds that live and migrate at altitude. J Appl Physiol 2017; 123: 942-950. 

[98] Senner, N. R., Stager, M., Verhoeven, M. A., Cheviron, Z. A., Piersma, T., Bouten, W. (2018). High-altitude shorebird migration in the absence of topographical barriers: avoiding high air temperatures and searching for profitable winds. Proc. R. Soc. B, 2018; 285: 20180569. 

[99] Rueden, C. T., Schindelin, J., Hiner, M. C., DeZonia, B. E., Walter, A. E., Arena, E. T., Eliceiri, K. W. (2017). ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinfornatics, 2017; 18: 529.

[100]  Frank, J., Radermacher, M., Pencze, P., Zhu, J., Li, Y., Ladjadj, M., Leith, A. (1996). SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol, 1996; 116: 190-199.

[101]  Maina, J. N., Woodward, J. D. (2009). Three-dimensional serial section computer reconstruction of the arrange-ment of the structural components of the parabronchus of the ostrich, Struthio camelus lung. Anat Rec., 2009; 292: 1685-1698.

[102]  Rau, T. S., Hussong, A., Herzog, A., Majdani, O., Lenarz, T., Leinung, M. (2011). Accuracy of computer-aided geometric 3D reconstruction based on histological serial microgrinding preparation. Comput Methods Biomech Biomed Engineer, 2011; 14: 581-594.

[103]  Pintilie, G. D., Zhang, J., Goddard, T. D., Chiu, W., Gossard, D. C. (2010). Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions. J Struct Biol, 2010; 170: 427-38.

[104]  Pattersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., Ferrin, T. E. (2004). UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem, 2004; 5: 1605-1612.

[105]  Abdalla, M. A. (1989). The blood supply to the lung. In: Form and function in birds, vol. 4 (King AS, McLelland J eds). San Diego; Academic Press; 1989: pp. 281-306.

[106]  Abdalla, M. A., King, A. S. (1975). The functional anatomy of the pulmonary circulation of the domestic fowl. Respir Physiol, 1975; 23: 267-290.

[107]  Abdalla, M. A., King, A. S. (1976). Pulmonary arteriovenous anastomoses in the avian lung: do they exist. Respir Physiol, 1976; 27: 187-191.

[108]  Abdalla, M. A., King, A. S. (1976). The functional anatomy of the bronchial circulation of the domestic fowl. J Anat, 1976; 121: 537-550.

[109]  Abdalla, M. A., King, A. S. (1977). The avian bronchial arteries: species variations. J Anat, 1977; 123: 697-704.

[110]  King, A. S. (1966). Structural and functional aspects of the avian lung and its air sacs. Internat J Rev Gen Exp Zool, 1966; 2: 171-267.

[111]  Maina, J. N. (1982). A scanning electron microscopic study of the air and blood capillaries of the lung of the do-mestic fowl (Gallus domesticus). Experientia, 1982; 35: 614-616. 

[112]  Maina, J. N. (1988). Scanning electron microscopic study of the spatial organization of the air- and the blood con-ducting components of the avian lung, Gallus gallus variant domesticus. Anat Rec., 1988; 222: 145-153.

[113]  Makanya, A. N., Kavoi, B. M., Djonov, V. (2014). Three-dimensional structure and disposition of the air conduct-ing and gas exchange conduits of the avian lung: the domestic duck (Cairina moschata). J Anat, 2014; 1: 1-9.

[114]  West, N. H., Bamford, O. S., Jones, D. R. (1977). A scanning electron microscope study of the microvasculature of the avian lung. Cell Tissue Res, 1977; 176: 553-564.

[115]  Makanya, A. N., Djonov, V. (2008). Development and spatial organization of the air conduits in the lung of the domestic fowl, Gallus variant domesticus. Microsc Res Tech, 2008; 71: 689-702.

[116]  Makanya, A. N., Djonov, V. (2009). Parabronchial angioarchitecture in developing and adult chickens. J Appl Physiol, 2009; 106: 1959-69.

[117]  Pandey, A. K., Praveen, P. K., Ganguly, S., Para, P. A., Wakchaure, R., Saroj, K., Mahajan, T. (2015). Avian res-piratory and physiology with its interspecies variations: a review. World J Pharmacol Life Sci, 2015; 1: 137-148.

[118]  Radu, C., Radu, L. (1971). Le dispositive vasculaire du poumon chez les oiseaux domestiques. Revue de Medecine Veterinaire, 1971; 122: 1219-1226.

[119]  Weibel, E. R. (1984). The pathway for oxygen: structure and function in the mammalian respiratory system. Cambridge (MA); Harvard University Press: 1984.

[120]  Schittny, J., Burri, P. H. (2003). Morphogenesis of the mammalian lung: aspects of structure and extracellular ma-trix. In: Lung development and regeneration (Massaro DJ, Massaro GC, Chambon P eds). New York; Marcel; 2003: pp. 275-316.

[121]  Moura, R. S., Correia-Pinto, J. (2017). Molecular aspects of avian lung development. In: The biology of the avian respiratory system: evolution, development, structure and function (Maina JN ed). Berlin; Springer; 2017: pp. 129-146.

[122]  Duncker, H. R. (1978). Development of the avian respiratory and circulatory systems. In: Respiratory  function in birds, adult and embryonic (Duncker HR ed). Berlin; Springer; 1978: pp. 260-273.

[123]  Maina, J. N. (2003). A systematic study of the development of the airway (bronchial) system of the avian lung from days 3 to 26 of embryogenesis: a transmission electron microscopic study of the domestic fowl, Gallus gallus variant domesticus. Tissue Cell, 2003; 35: 375-391. 

[124]  Maina, J. N. (2003). Developmental dynamics of the bronchial- (airway) and air sac systems of the avian respira-tory system from days 3 to 26 of life: a scanning electron microscopic study of the domestic fowl, Gallus gallus variant domesticus. Anat Embryol, 2003; 207: 119-134.

[125]  Burri, P. H. (1984). Fetal and postnatal development of the lung. Ann Rev Physiol, 1984; 46: 617-628. 

[126]  Burri, P. H. (1985). Development and growth of the human lung. In: Handbook of physiology, section 3: the res-piratory system (Fishman AP, Fisher AB eds). Bethesda (MD); American Physiological Society; 1985: pp. 1-46. 

[127]  Hughes, L. C., Archer, C. W., Gwynn, I. (2005). The ultrastructure of mouse articular cartilage: collagen orienta-tion and implications for tissue functionality. A polarised light and scanning electron microscope study and review. Europ Cells Materials, 2005; 9: 68-84. 

[128]  Woodward, J. D., Wepf, R., Sewell, B. T. (2009). Three-dimensional reconstruction of biological macromolecular complexes from in-lens scanning electronmicro-graphs. J Microsc, 2009; 234: 287-292.

[129]  Peddie, C. J., Collinson, L. M. (2014). Exploring the third dimension: volume electron microscopy comes of age. Micron, 2014; 61: 9-19.

How to cite this paper

3D Computer Reconstruction of the Airway and the Vascular Systems of the Lung of the Domestic Fowl, Gallus gallus Variant domesticu

How to cite this paper: John N. Maina, Yolanda Ramonisi, Reatlegile Mashiteng, Lolo Mokae, Jeremy D. Woodward. (2021) 3D Computer Reconstruction of the Airway and the Vascular Systems of the Lung of the Domestic Fowl, Gallus gallus Variant domesticuJournal of Applied Mathematics and Computation5(2), 89-104.

DOI: http://dx.doi.org/10.26855/jamc.2021.06.004