The avian respiratory system: a unique model for studies of respiratory toxicosis and for monitoring air quality The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Brown, R E, J D Brain, and N Wang. 1997. “The Avian Respiratory System: a Unique Model for Studies of Respiratory Toxicosis and for Monitoring Air Quality.” Environmental Health Perspectives 105 (2) (February 1): 188–200. doi:10.1289/ehp.97105188. Published Version doi:10.1289/ehp.97105188 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:32683869 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Research RetI e Revievvs The Avian Respiratory System: A Unique Model for Studies of Respiratory Toxicosis and for Monitoring Air Quality Richard E. Brown, Joseph D. Brain, and Ning Wang Physiology Program, Department of Environmental Health, Harvard School of Public Health, Boston, MA 02115 USA the avian respiratory system is to add to our .~~~~~~~~~~~~~~~~~~. ..... ... There a distinct dandm understanding of respiratory toxicosis, if we bird's lung-irsa resraorys d the mm bg In thi papr, are to maintain the health of birds in agri- we review physiologf the avia spi e with tO oe inisms cultural and wild settings, and if birds are to that may lad to signifitly diret ults, eate .totse in _mm, f i eosre become valuable monitors of air quality, to toxic gaseai:_d airbore p . We s. n C dbe then we must study the pathophysiology of e..xp.loimdto ther our understanding of thebasii ..... d ... olg......a.d a broad range of toxic gases and airborne part~cuIae) The larg niass-pd isa ah......gs. ut:t..' particulates in a wide variety of species. cdafy dunngm;:reise could be epotdasaenv ontrcarmmiy id hav iu&u offer in our of respiratory cx realiedtby Functional Morphology of the investigating, in a wide variety ofavian the oloc n onse a b Avian Respiratory System of wl ozants on the bird's unique rspa sym. Kiyw anatomy, birds, s uptake, kpat deposition, physiology, i ilog, vantilatiion En'Exi Hsalth Anatomy ofthe avian lung-ar-sac Pmp (OM88200(19) system Upper respiratory tract. The bird's respira- tory tract cranial to the tracheal bifurcation To what extent do the pathophysiologic sity demands that we also understand the is qualitatively similar to that of mammals; effects of inhaled substances, gaseous and interactions between the bird's unique respi- it has a nasal cavity with communicating particulate, depend on the particular struc- ratory system, gas uptake, and the patho- sinuses, a larynx supported by cartilaginous tural and physiologic features of an animal's physiologic effects of contaminating toxic plates, and a tracheal lumen supported by respiratory system? The anatomy, physiolo- gases and airborne particulates. Birds such cartilaginous or ossified rings. However, the gy, and mechanics of the avian respiratory as chickens and turkeys represent an impor- length of the bird's trachea is, on average, system are distinctly different from that of tant and expanding source ofanimal protein 2.7 times that ofcomparably sized mammals mammals (1). We suggest that, due to their for human nutrition. The environment (6). A small increase in tracheal diameter unique respiratory apparatus, birds may within modern poultry and egg production (1.29 times that of comparably sized mam- represent valuable experimental models in facilities, in which birds are densely housed, mal) ameliorates any increases in resistance the study of respiratory toxicosis. Such commonly exposes birds to high levels of to flow expected from the considerably comparative knowledge concerning the aerosolized particulates and toxic gases such longer trachea. Although the bird's trachea pathophysiology of inhaled substances may as ammonia and methane. Surprisingly, lit- is lined with a secretory (mucous), ciliated offer insights otherwise not available. Here de research has been carried out in birds on epithelium, there is no information about we describe the structure, ventilation, and gas uptake (other than 02 and CO2), parti- the performance of the mucociliary trans- gas flow pattern of the bird's lung-air-sac cle deposition, and the toxicity and patho- port mechanism. Further, there are a few system relative to the analogous features, if physiology ofinhaled substances. avian taxa (e.g., swans, cranes, birds of par- any, of the mammalian bronchoalveolar Toxic gases and/or airborne particulates adise) that have tracheal lengths up to four lung. We point out those anatomical and contaminate the environment and can have times that of comparably sized birds, the physiologic features of the bird's respiratory debilitating or destructive effects on birds redundant coils of which are considered apparatus that may produce significantly (and other wildlife) via a variety ofdistribu- adaptations for phonation (7). Tracheal different responses from the normal tion modes (e.g., air or water) and bio- lengths 10 times that of comparably sized response to inhaled substances, gases, and chemical mechanisms (2-5). Here we are particulates in mammals. concerned only with those gaseous and par- Address correspondence to N. Wang, Physiology Concems about the hazardous effects of ticulate contaminants that enter the bird Program, Department of Environmental Health, gas and particle emissions from expanding via its respiratory tract, of which little is Harvard School of Public Health, 665 Huntington industrial and agricultural (and natural) known or understood. Ifwe understood the Avenue, Boston, MA 02115 USA. RE. Brown is currently at Zoologiska Institutionen, sources supporting a burgeoning population pathophysiology of inhaled environmental Zoomorfologiska Avdedningen, Goteborg Universitt, have led to considerable efforts toward contaminants (gas and particulate) on birds S-413-90, G6teborg, Sweden. understanding the effects of air quality on (adult and embryonic), they could serve as Received 20 August 1996; accepted 5 November human health. Maintenance ofnatural diver- sensitive, direct monitors of air quality. If 1996. 188 Volume 105, Number 2, February 1997 * Environmental Health Perspectives Reviews * Avian respiratory toxicology mammals suggest the need ofpossible novel mechanisms to assist in dearance. In sharp contrast to the C-shaped carti- laginous rings supporting the tracheal lumen ofmammals, the bird's tracheal rings are complete (i.e., 0-shaped and commonly ossified). In the mammalian trachea, the collapsible membrane spanning the gap between the ends of the incomplete tracheal rings is considered an important feature of the dearance mechanism ofthe mammalian cough (8). Although birds do perform a coughlike action, we do not know if such behavior represents an effective mechanism for clearing debris from their longer tra- cheas. And if such a dearance mechanism exists, what are the mechanics involved? The avian vocal apparatus, the syrinx, is located at the point the main stem bronchi diverge from the caudal trachea (Fig. 1). At that site there are significant departures Fgure 1. Diagram of the components of the avian lung-air-sac respiratory system. From the bird's intrapul- monary primary bronchus (Bronchus primarius, pars intrapulmonalis) arise two clusters of secondary from the round geometry ofthe trachea and bronchi: from its cranial end arise four ventrobronchi (Bronchi medioventrales), and, prior to its termination at main stem bronchi which may influence the orifice of the abdominal air sac, arise the 8-14 dorsobronchi (Bronchi mediodorsales) and the latero- particle deposition. bronchus (LB) (Bronchi lateroventrales), which connects the caudal thoracic air sac to the intrapulmonary Bronchial system. Whereas the mam- bronchus. The constant-volume gas-exchange area of the avian lung-air-sac system, i.e., the parabronchi malian bronchial system ramifies (23 gen- (for simplicity only a few are shown), is connected between dorsobronchi and ventrobronchi and is ventilated erations) like the roots of a tree throughout unidirectionally (arrows). The several air sacs are the sites of volume expansion and act as bellows to move the pulmonary parenchyma (Fig. 2), the gas through the bird's lung (parabronchi). [Modified from Wang et al., (38); reprinted with permission from bird's primary bronchus extending from John Wiley & Sons, Inc.] tracheal bifurcation to the ostium of the abdominal air sac has only two dusters of secondary bronchi (Fig. 1). From the cra- nial end of the bird's intrapulmonary pri- mary bronchus arise 4 approximately equal-sized ventrobronchi, and from its caudal segment arise 7-14 variably sized dorsobronchi and a variable number (<6) of laterobronchi. The epithelium lining the primary bronchi and the initial segments of the secondary bronchi is similar to that seen in larger mammalian airways: pseu- dostratified ciliated epithelium with mucous-secreting goblet cells. The mammalian bronchial system ter- minates in myriad (300 million in Homo) small, blind-end alveoli, which are the site of gas exchange and volume (tidal) expan- sion. In sharp contrast, birds have a nearly constant volume, flow-through lung in which the site ofgas exchange is the parallel Figure 2. Bronchial tree of the human lung, latex cast, ventral view, left lung. The caudal trachea (large asterisk) gives rise to the primary