Abstract
Collectively coordinated ciliary activity propels the airway mucus, which lines the luminal surface of the vertebrate respiratory system, in cranial direction. Our contemporary understanding on how the quantitative characteristics of the metachronal wave field determines the resulting mucociliary transport is still limited, partly due to the sparse availability of quantitative observational data. We employed high-speed video reflection microscopy to image and quantitatively characterize the metachronal wave field as well as the mucociliary transport in excised bovine, porcine, ovine, lapine, turkey and ostrich samples. Image processing techniques were used to determine the ciliary beating frequency (CBF), the velocity and wavelength of the metachronal wave and the mucociliary transport velocity. The transport direction was found to strongly correlate with the mean wave propagation direction in all six species. The CBF yielded similar values (10–15 Hz) for all six species. Birds were found to exhibit higher transport speeds (130–260 upmum/s) than mammals (20–80 upmum/s). While the average transport direction significantly deviates from the tracheal long axis in mammals, no significant deviation was found in birds. The metachronal waves were found to propagate at about 4–8 times the speed of mucociliary transport in mammals, whereas in birds they propagate at about the transport speed. The mucociliary transport in birds is fast and roughly follows the TLA, whereas the transport is slower and proceeds along a left-handed spiral in mammals. The longer wavelengths and the lower ratio between the metachronal wave speed and the mucociliary transport speed provide evidence that the mucociliary clearance mechanism operates differently in birds than in mammals.
Highlights
IntroductionWhen examining the literature on the respiratory mucociliary clearance system (e.g. see Sleigh et al 1988; Satir and Sleigh 1990; Priel 1997; Houtmeyers et al 1999; Wanner et al 1996; Salathe 2001; Stannard and O’Callaghan 2006; Satir and Christensen 2007; Salathe 2007; Smith et al 2008; Norton et al 2011; Elgeti and Gompper 2013; BrumleyAndreas Burn and Martin Schneiter contributed to this article, they were co-first authors.1 3 Vol.:(0123456789)European Biophysics Journal (2022) 51:51–65One major reason for our limited knowledge is the lack of adequate observations under native conditions in the respiratory tract
The reliability of such indirect observation became questioned and the research focused on transparent models, which are accessible by transmission microscopy, such as epithelial sheets from frog pharyngal or esophagal epithelium (Wilson et al 1975; Eshel and Priel 1987; Gheber and Priel 1994), cultured rabbit tracheal epithelium (Cheung and Jahn 1976; Sanderson and Sleigh 1981; Romet et al 1991) or cultures from human biopsies (Marino and Aiello 1982; Rautiainen et al 1992; Hard et al 1999; Chilvers and O’Callaghan 2000)
We developed a set of techniques and algorithms that allowed us to simultaneously measure the mucociliary transport velocity and the space-time structure of the metachronal wave field on excised, but otherwise unaltered, tracheas under close-to-native environmental conditions
Summary
When examining the literature on the respiratory mucociliary clearance system (e.g. see Sleigh et al 1988; Satir and Sleigh 1990; Priel 1997; Houtmeyers et al 1999; Wanner et al 1996; Salathe 2001; Stannard and O’Callaghan 2006; Satir and Christensen 2007; Salathe 2007; Smith et al 2008; Norton et al 2011; Elgeti and Gompper 2013; BrumleyAndreas Burn and Martin Schneiter contributed to this article, they were co-first authors.1 3 Vol.:(0123456789)European Biophysics Journal (2022) 51:51–65One major reason for our limited knowledge is the lack of adequate observations under native conditions in the respiratory tract. Under native conditions the dominant source of contrast is the reflection from the air-mucus interface (see Iravani and Melville 1976 and references therein) The reliability of such indirect observation became questioned and the research focused on transparent models, which are accessible by transmission microscopy, such as epithelial sheets from frog pharyngal or esophagal epithelium (Wilson et al 1975; Eshel and Priel 1987; Gheber and Priel 1994), cultured rabbit tracheal epithelium (Cheung and Jahn 1976; Sanderson and Sleigh 1981; Romet et al 1991) or cultures from human biopsies (Marino and Aiello 1982; Rautiainen et al 1992; Hard et al 1999; Chilvers and O’Callaghan 2000). It has been shown that an increase of the viscosity of the tissue culture medium (from 20 to 1500 cp) may change the metachronism in cultured frog esophagus from diaplectic to orthoplectic (Gheber et al 1998)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
