Particle Clearance in Human Bronchial Airways: Comparison of Stochastic Model Predictions with Experimental Data

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1 Ann. occup. Hyg., Vol. 46, Supplement 1, pp , British Occupational Hygiene Society Published by Oxford University Press DOI: /annhyg/mef659 Particle Clearance in Human Bronchial Airways: Comparison of Stochastic Model Predictions with Experimental Data R. STURM 1, W. HOFMANN 1 *, G. SCHEUCH 2, K. SOMMERER 2, P. CAMNER 3 and M. SVARTENGREN 3,4 1 Institute of Physics and Biophysics, University of Salzburg, Hellbrunner Strasse 34, A-5020 Salzburg, Austria; 2 InAMed, Taunus Strasse 12, D Gemuenden, Germany; 3 Institute of Environmental Medicine and 4 Department of Public Health Sciences, Karolinska Institute, S Stockholm, Sweden A stochastic bronchial clearance model has been developed that is based on a probabilistic asymmetric structure of the human lung. This model takes mucociliary transport rates to be a function of airway diameter, considers delayed mucus clearance at bifurcation sites, and uses an empirically derived expression for the slow clearance fraction as a function of particle diameter. For the calculation of retention curves, this bronchial clearance model was applied to predicted deposition patterns for different particle sizes and breathing conditions. Two sets of experimental data were used: (i) bolus inhalation at different volumetric depths, and (ii) extremely slow inhalation, providing a wide range of initial deposition patterns. In general, excellent agreement was found between theoretical predictions and experimental retention data (short-term retention curves and 24 h retention values) for different particle sizes, with maximum differences between 10 and 20%. Two different mechanisms are discussed to interpret the experimentally observed relation between the slow clearance fraction and particle diameter. Keywords: human lung; mucociliary clearance; particle retention; slow bronchial clearance INTRODUCTION Results of bolus inhalation experiments have suggested the existence of a slow bronchial clearance phase, exhibiting a distinct dependence on particle size (Stahlhofen, 1989; Scheuch and Stahlhofen, 1992). To investigate potential underlying mechanisms, the objectives of the present study were (i) to calculate short-term retention curves for different particle sizes, (ii) to compare them with the available experimental evidence, and (iii) to identify specific mechanisms for the slow bronchial clearance phase The retention calculations presented here are based on a stochastic bronchial clearance model. This model takes mucociliary transport rates to be a function of airway diameter, considers delayed mucus clearance at bifurcation sites, and uses an empirically derived expression for the slow clearance fraction as a function of particle diameter. For the calculation of *Author to whom correspondence should be addressed. Tel: ; fax: ; werner.hofmann@sbg.ac.at retention curves, this bronchial clearance model was applied to predicted deposition patterns for different particle sizes and breathing conditions and compared to two sets of experimental data: (i) bolus inhalation at different volumetric depths (Stahlhofen, 1989; Scheuch and Stahlhofen, 1992), and (ii) extremely slow inhalation (Philipson et al., 2000), thereby providing a wide range of initial deposition patterns. MATERIALS AND METHODS Bronchial clearance model The stochastic particle deposition model of Koblinger and Hofmann (1990) was extended by incorporating a bronchial clearance model which allows the calculation of particle retention within an asymmetrically branching tracheobronchial tree. Calculations of particle clearance by the mucociliary escalator are based on a positive correlation between airway diameter and mucus velocity in that airway, normalized to a measured tracheal mucus velocity of 5.5 mm/min (ICRP, 1994). Stochastically generated mucus vel- 329

2 330 R. Sturm et al. (a) (b) Fig. 1. (a) Comparison of mucus velocities calculated with the stochastic clearance model and the deterministic clearance model of Lee et al. (1979). (b) Dependence of average mucus velocities on average diameters of the human bronchial airway generations. ocities decrease in an almost exponential manner with increasing generation number (Fig. 1a), differing by <10% from the values reported by Lee et al. (1979) for a deterministic, symmetric lung. As illustrated in Fig. 1b, the relationship between computed average mucus velocities and airway diameters can be reasonably approximated by an exponential function. Since our present understanding of the mechanisms underlying slow bronchial clearance is still fragmentary, experimental data obtained by bolus experiments were used to derive an empirical relationship between the slow clearance fraction f s (fraction retained after 24 h) and the geometric particle diameter, d geom (µm): f s = d geom (1) indicating that only particles smaller than ~6.5 µm experience a slow bronchial clearance. The delay of mucus flow at carinal ridges is considered in our model by an adjustable average delay time t, which is selected randomly from a uniform distribution between 0 and t. At present, a default value of 10 min is used in the program. Experimental data Two sets of experimental clearance data were used for the comparison with predicted retention curves: (i) bolus inhalation at different volumetric depths (Stahlhofen, 1989; Scheuch and Stahlhofen, 1992), and (ii) extremely slow inhalation (Philipson et al., 2000). Applying the bolus technique, the retention of monodisperse 111 In-labelled polystyrene particles (d = 6.7 µm) was measured at different times after bolus inhalation. The volumetric bolus front depth V F varied between 54.6 and ml to target different regions of the bronchial tree. To investigate the dependence of particle retention on particle size, monodisperse aerosols with diameters of 1.7, 3.2 and 6.7 µm were injected as shallow boluses with a front depth of ~100 ml and a half-width between 40 and 50 ml. The philosophy of the extremely slow inhalation technique with a flow rate of l/s is to specifically increase deposition in small bronchiolar airways of the tracheobronchial tree (Philipson et al., 2000). To investigate slow thoracic clearance, volunteers inhaled 111 In-labelled polystyrene particles (d = 6.05 µm, 1.05 g/cm 3 ). The radioactivity in the thorax

3 Particle clearance in human bronchial airways 331 Fig. 2. Results of the stochastic clearance calculations. (a) Retention curves of 6.7 µm particles for different volumetric bolus front depths. (b) Comparison between measured and predicted 24 h retention values of 6.7 µm particles for different volumetric bolus front depths. (c) Measured and predicted retention curves for different particle sizes in shallow boluses. (d) 24 hour retention values was measured immediately after inhalation and at selected times between 24 h and 2 weeks. RESULTS Simulation of the bolus experiments In general, excellent agreement was found between theoretical predictions and experimental retention data (short-term retention curves and 24 h retention values) for different particle sizes, with maximum differences between 10 and 20%. As illustrated in Fig. 2a,b, the A-values (i.e. fraction retained after 24 h) of the experimentally derived retention curves for 6.7 µm particles exhibit a positive correlation with the volumetric bolus front depths, increasing from 0% for V F = 54.6 ml to 85% for V F = ml. For comparison, predicted A-values range from 0 to 76%. Shallow bolus experiments with different particle sizes (1.7, 3.2 and 6.7 µm) indicate a positive correlation between particle diameter and short-term retention (Fig. 2c). While >80% of the 6.7 µm particles are cleared from the tracheobronchial tree within the first 10 h after inhalation, only 20% of the deposited 1.7 µm particles leave the thorax during that time interval. Differences between predicted and measured data are again rather small, with a maximum of ~10%. Simulation of extremely slow inhalation experiments In their experiments, Philipson et al. (2000) observed a mean retention value after 24 h of 51 ± 5% for 6.05 µm particles (Fig. 2d). Corresponding experiments with a flow rate of 0.5 l/s yielded an A-value of 46 ± 11%. Simulation of these experiments with our clearance model produced A-values of 45 and 49%, thus agreeing very well with the experimental data. When extended to intermediate and very high flow rates, the clearance model predicts a slightly convex curve between and 0.5 l/s with a maximum at ~0.2 l/s (Fig. 2d), which has to be tested in future experiments. However, the main objective of that experiment was to study whether the slow bronchial clearance fraction depends on geometric or aerodynamic particle diameter (see equation 1). In contrast

4 332 R. Sturm et al. Fig. 3. Possible mechanisms responsible for slow bronchial clearance. (a) Particle capture in the sol phase after penetration through the gel layer. (b) Particle capture in the sol phase after direct deposition in mucus discontinuities (i.e. no gel layer). (c) Mucus delay at carinal ridges of airway bifurcations. to the bolus experiments discussed above, 24 h retention in this study did not depend on the geometric diameter. DISCUSSION Comparison with experimental retention curves indicates that the stochastic clearance model in its present formulation provides fair fits to both bolus and extremely slow inhalation data covering a wide range of initial deposition patterns. While the dependence of the slowly cleared fraction on particle size is expressed by an empirically derived linear equation, further refinement of the model will require a mechanistic understanding of potential mechanisms. At the moment, our mechanistic understanding of the slow clearance phase is mainly based on the results of Gehr et al. (1991), who found evidence for the capture of particles in the sol layer of the bronchial epithelium, assuming that they have passed through the gel layer (Fig. 3a). As these authors used only rather large particles (d = 6 µm), we do not have any comparable evidence for smaller particles. Recently, however, the penetration of the mucus layer was questioned by Podgorski and Sosnowski (2000) on theoretical grounds. An alternative mechanism of slow bronchial clearance is based on experimental findings (e.g. Mercer et al., 1992) that the mucus layer, particularly in the smaller airways, is not continuous but patchy. Particles being deposited in such holes (i.e. no gel layer) of a discontinuous mucus layer (Fig. 3b) may experience longer residence times than those initially deposited on the gel layer. Hence the slow clearance fraction may be interpreted as the probability of hitting such a hole which depends, among other parameters, on particle size. Mucus delay at bifurcations (Fig. 3c) due to local fluid dynamics or impairment of ciliary movement may be an additional effect contributing to slow bronchial clearance (Hofmann et al., 1990).

5 Particle clearance in human bronchial airways 333 Acknowledgements This research was supported in part by the Commission of the European Communities, contract no. FIGD- CT REFERENCES Gehr P, Im Hof V, Geiser M, Schürch S. (1991) The fate of particles deposited in the intrapulmonary conducting airways. J Aerosol Med; 1: Hofmann W, Martonen TB, Ménache MG. (1990) A dosimetric model for localized radon progeny accumulations at tracheobronchial bifurcations. Radiat Protect Dosim; 30: ICRP. (1994) Human respiratory tract model for radiological protection. International Commission on Radiological Protection (ICRP) Publication 66, Ann ICRP; 24: 1 3. Oxford: Elsevier. Koblinger L, Hofmann W. (1990) Monte Carlo modeling of aerosol deposition in human lungs. Part I: Simulation of particle transport in a stochastic lung structure. J Aerosol Sci; 21: Lee PS, Gerrity TR, Hass FJ, Lourenco RV. (1979) A model for tracheobronchial clearance of inhaled particles in man and a comparison with data. IEEE Trans Biomed Eng; 26: Mercer RR, Russell ML, Crapo JD. (1992) Mucous lining layers in human and rat airways. Annu Rev Respir Dis; 145: 355. Philipson K, Falk R, Svartengren M et al. (2000) Does lung retention of inhaled particles depend on their geometric diameter? Exp Lung Res; 26: Podgorski A, Sosnowski TR. (2000) Dynamic analysis of the process of an aerosol particle deposition onto an extracellular lining layer in the human lung. J Aerosol Sci; 31 (suppl. 1): Scheuch G, Stahlhofen W. (1992) Deposition and dispersion of aerosol particles in the airways of the human respiratory tract: the effect of particle size. Exp Lung Res; 18: Stahlhofen W. (1989) Human lung clearance following bolus inhalation of radioaerosols. In Crapo JD, Smolko ED, Miller FJ, Graham JA, Hayes AW, editors. Extrapolation of dosimetric relationships for inhaled particles and gases. San Diego: Academic Press. pp

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