In an effort to understand the fate of inhaled submicron particles in the small sacs, or alveoli, comprising the gas-exchange region of the lung, we calculated the flow in three-dimensional (3D) rhythmically expanding models of alveolated ducts. Since convection toward the alveolar walls is a precursor to particle deposition, it was the goal of this paper to investigate the streamline maps’ dependence upon alveoli location along the acinar tree. On the alveolar midplane, the recirculating flow pattern exhibited closed streamlines with a stagnation saddle point. Off the midplane we found no closed streamlines but nested, funnel-like, spiral, structures (reminiscent of Russian nesting dolls) that were directed towards the expanding walls in inspiration, and away from the contracting walls in expiration. These nested, funnel-like, structures were surrounded by air that flowed into the cavity from the central channel over inspiration and flowed from the cavity to the central channel over expiration. We also found that fluid particle tracks exhibited similar nested funnel-like spiral structures. We conclude that these unique alveolar flow structures may be of importance in enhancing deposition. In addition, due to inertia, the nested, funnel-like, structures change shape and position slightly during a breathing cycle, resulting in flow mixing. Also, each inspiration feeds a fresh supply of particle-laden air from the central channel to the region surrounding the mixing region. Thus, this combination of flow mixer and flow feeder makes each individual alveolus an effective mixing unit, which is likely to play an important role in determining the overall efficiency of convective mixing in the acinus.

References

1.
Haefeli-Bleuer
,
B.
, and
Weibel
,
E. R.
,
1988
, “
Morphometry of the Human Pulmonary Acinus
,”
Anatomical Rec.
,
220
(
4
), pp.
401
414
.10.1002/ar.1092200410
2.
ICRP Publication 66
,
1994
, “
Human Respiratory Tract Model for Radiological Protection
,”
A report of a Task Group of the International Commission on Radiological Protection, Ann. ICRP
,
24
(
1–3
), pp.
1
482
.
3.
Tsuda
,
A.
,
Otani
,
Y.
, and
Butler
,
J. P.
,
1999
, “
Acinar Flow Irreversibility Caused by Boundary Perturbation of Reversible Alveolar Wall Motion
,”
J. Appl. Physiol.
,
86
(
3
), pp.
977
984
.
4.
Tsuda
,
A.
,
Rogers
,
R. A.
,
Hydon
,
P. E.
, and
Butler
,
J. P.
,
2002
, “
Chaotic Mixing Deep in the Lung
,”
Proc. Natl. Acad. Sci. U.S.A.
,
99
, pp.
10173
10178
.10.1073/pnas.102318299
5.
Tippe
,
A.
, and
Tsuda
,
A.
,
2000
, “
Recirculating Flow in an Expanding Alveolar Model: Experimental Evidence of Flow-Induced Mixing of Aerosols in the Pulmonary Acinus
,”
J. Aerosol Sci.
,
31
(
8
), pp.
979
986
.10.1016/S0021-8502(99)00572-8
6.
Tsuda
,
A.
,
Henry
,
F. S.
, and
Butler
,
J. P.
,
1995
, “
Chaotic Mixing of Alveolated Duct Flow in Rhythmically Expanding Pulmonary Acinus
,”
J. Appl. Physiol.
,
79
(
3
), pp.
1055
1063
.
7.
Haber
,
S.
,
Butler
,
J. P.
,
Brenner
,
H.
,
Emanuel
,
I.
, and
Tsuda
,
A.
,
2000
, “
Flow Field in Self-Similar Expansion on a Pulmonary Alveolus During Rhythmical Breathing
,”
J. Fluid Mech.
,
405
, pp.
243
268
.10.1017/S0022112099007375
8.
Henry
,
F. S.
,
Butler
,
J. P.
, and
Tsuda
,
A.
,
2002
, “
Kinematically Irreversible Flow and Aerosol Transport in the Pulmonary Acinus: A Departure From Classical Dispersive Transport
,”
J. Appl. Physiol.
,
92
, pp.
835
845
.
9.
Henry
,
F. S.
, Laine-Pearson
,
F. E.
, and
Tsuda
,
A.
,
2009
, “
Hamiltonian Chaos in a Model Alveolus
,”
ASME J. Biomech. Eng.
,
131
(
1
), p.
011006
.10.1115/1.2953559
10.
Henry
,
F. S.
, and
Tsuda
,
A.
,
2010
, “
Radial Transport Along the Human Acinar Tree
,”
ASME J. Biomech. Eng.
,
132
(
10
), p.
101001
.10.1115/1.4002371
11.
Tsuda
,
A.
,
Laine-Pearson
,
F. E.
, and
Hydon
,
P. E.
,
2011
, “
Why Chaotic Mixing of Particles Is Inevitable in the Deep Lung
,”
J. Theor. Biol.
,
286
, pp.
57
66
.10.1016/j.jtbi.2011.06.038
12.
Berg
,
E. J.
,
Weisman
,
J. L.
,
Oldham
,
M. J.
, and
Robinson
,
R. J.
,
2010
, “
Flow Field Analysis in a Compliant Acinus Replica Model Using Particle Image Velocimetry (PIV)
,”
J. Biomech.
,
43
(
6
), pp.
1039
1047
.10.1016/j.jbiomech.2009.12.019
13.
Berg
,
E. J.
, and
Robinson
,
R. J.
,
2011
, “
Stereoscopic Particle Image Velocimetry Analysis of Healthy and Emphysemic Alveolar Sac Models
,”
J. Biomech. Eng.
,
133
(
6
), p.
061004
.10.1115/1.4004251
14.
Chhabra
,
S.
, and
Prasad
,
A. K.
,
2010
, “
Flow and Particle Dispersion in a Pulmonary Alveolus—Part I: Velocity Measurements and Convective Particle Transport
,”
J. Biomech. Eng.
,
132
(
5
), p.
051009
.10.1115/1.4001112
15.
Chhabra
,
S.
, and
Prasad
,
A. K.
,
2010
, “
Flow and Particle Dispersion in a Pulmonary Alveolus—Part II: Effect of Gravity on Particle Transport
,”
J. Biomech. Eng.
,
132
(
5
), p.
051010
.10.1115/1.4001113
16.
Oakes
,
J. M.
,
Day
,
S.
,
Weinstein
,
S. J.
, and
Robinson
,
R. J.
,
2010
, “
Flow Field Analysis in Expanding Healthy and Emphysematous Alveolar Models Using Particle Image Velocimetry
,”
J. Biomech. Eng.
,
132
(
2
), p.
021008
.10.1115/1.4000870
17.
Harding
,
E. M.
, Jr.
, and
Robinson
,
R. J.
,
2010
, “
Flow in a Terminal Alveolar Sac Model With Expanding Walls Using Computational Fluid Dynamics
,”
Inhal. Toxicol.
,
22
(
8
), pp.
669
678
.10.3109/08958371003749939
18.
Kumar
,
H.
,
Tawhai
,
M. H.
,
Hoffman
,
E. A.
, and
Lin
,
C. L.
,
2009
, “
The Effects of Geometry on Airflow in the Acinar Region of the Human Lung
,”
J. Biomech.
,
42
(
11
), pp.
1635
1642
.10.1016/j.jbiomech.2009.04.046
19.
Kumar
,
H.
,
Tawhai
,
M. H.
,
Hoffman
,
E. A.
, and
Lin
,
C. L.
,
2011
, “
Steady Streaming: A Key Mixing Mechanism in Low-Reynolds-Number Acinar Flows
,”
Phys. Fluids
,
23
(
4
), p.
041902
.10.1063/1.3567066
20.
Ma
,
B.
, and
Darquenne
,
C.
,
2011
, “
Aerosol Deposition Characteristics in Distal Acinar Airways Under Cyclic Breathing Conditions
,”
J. Appl. Physiol.
,
110
(
5
), pp.
1271
1282
.10.1152/japplphysiol.00735.2010
21.
Sznitman
,
J.
,
Heimsch
,
F.
,
Heimsch
,
T.
,
Rusch
,
D.
, and
Rosgen
,
T.
,
2007
, “
Three-Dimensional Convective Alveolar Flow Induced by Rhythmic Breathing Motion of the Pulmonary Acinus
,”
ASME J. Biomech. Eng.
,
129
,
658
665
.10.1115/1.2768109
22.
Sznitman
,
J.
,
Heimsch
,
T.
,
Wildhaber
,
J. H.
,
Tsuda
,
A.
, and
Rösgen
,
T.
,
2009
, “
Respiratory Flow Phenomena and Gravitational Sedimentation in a Three-Dimensional Space-Filling Model of the Pulmonary Acinar Tree
,”
ASME J. Biomech. Eng.
,
131
(
3
), p.
031010
.10.1115/1.3049481
23.
Davies
,
C. N.
,
1972
, “
Breathing of Half-Micron Aerosols: II Interpretation of Experimental Results
,”
J. Appl. Physiol.
,
35
, pp.
605
611
.
24.
Taylor
,
G. I.
,
1967
,
Low Reynolds Number Flow
,
The National Committee for Fluid Mechanics Film, Encyclopaedia Britanica Education Corporation
.
25.
Davidson
,
M. R.
, and
Fitz-Gerald
,
J. M.
,
1972
, “
Flow Patterns in Models of Small Airway Units of the Lung
,”
J. Fluid Mech.
,
52
, pp.
161
177
.10.1017/S0022112072003015
26.
Filipovic
,
N.
,
Haberthür
,
D.
,
Henry
,
F. S.
,
Milasinovic
,
D.
,
Nikolic
,
D.
,
Schittny
,
J.
, and
Tsuda
,
A.
,
2010
, “
Recirculation Identified in a 3D Alveolar Duct Reconstructed Using Synchrotron Radiation Based X-Ray Tomographic Microscopy
,”
ATS meeting
,
New Orleans
(abstr.).
27.
Filipovic
,
N.
,
Henry
,
F. S.
,
Milasinovic
,
D.
, and
Tsuda
,
A.
,
2011
, “
Can Complex Alveolar Flow Patterns in Off Mid-Plane Trap Aerosol Particles?
,”
ATS meeting
,
Denver
(abstr.).
28.
Tsuda
,
A.
,
Filipovic
,
N.
,
Haberthür
,
D.
,
Dickie
,
R.
,
Matsui
,
Y.
,
Stampanoni
,
M.
, and
Schittny
,
J. C.
,
2008
, “
Finite Element 3D Reconstruction of the Pulmonary Acinus Imaged by Synchrotron X-Ray Tomography
,”
J. Appl. Physiol.
,
105
(
3
), pp.
964
976
.10.1152/japplphysiol.90546.2008
29.
Haberthür
,
D.
,
Hintermüller
,
C.
,
Marone
,
F.
,
Schittny
,
J. C.
, and
Stampanoni
,
M.
,
2010
, “
Radiation Dose Optimized Lateral Expansion of the Field of View in Synchrotron Radiation X-Ray Tomographic Microscopy
,”
J. Synchrotron Radiat.
,
17
(
5
), pp.
590
599
.10.1107/S0909049510019618
30.
Sznitman
,
J.
,
Sutter
,
R.
,
Altorfer
,
D.
,
Stampanoni
,
M.
,
Rösgen
,
T.
, and
Schittny
,
J. C.
,
2010
, “
Visualization of Respiratory Flows From 3D Reconstructed Alveolar Airspaces Using X-Ray Tomographic Microscopy
,”
J. Visualization
,
14
(
4
), pp.
337
345
.
31.
Tschanz
,
S. A.
,
Makanya
,
A. N.
,
Haenni
,
B.
, and
Burri
,
P. H.
,
2003
, “
Effects of Neonatal High-Dose Short-Term Glucocorticoid Treatment on the Lung: A Morphologic and Morphometric Study in the Rat
,”
Pediatr. Res.
,
53
(
1
), pp.
72
80
.10.1203/00006450-200301000-00014
32.
Luyet
,
C.
,
Burri
,
P. H.
, and
Schittny
,
J. C.
,
2002
, “
Suppression of Cell Proliferation and Programmed Cell Death by Dexamethasone During Postnatal Lung Development
,”
Am. J. Physiol. Lung Cellular Mol. Physiol.
,
282
(
3
), pp.
477
483
.10.1152/ajplung.00406.2000
33.
Stampanoni
,
M.
,
Groso
,
A.
,
Isenegger
,
G.
,
Mikuljan
,
G.
,
Chen
,
Q.
,
Bertrand
,
A.
,
Henein
,
S.
,
Betemps
,
R.
,
Frommherz
,
U.
,
Böher
,
P.
,
Meister
,
D.
,
Lange
,
M.
, and
Abela
,
R.
,
2006
, “
Trends in Synchrotron-Based Tomographic Imaging: The SLS Experience
,”
Proc. SPIE
,
6318
, p.
63180M
.10.1117/12.679497
34.
Filipovic
,
N.
,
Mijailovic
,
S.
,
Tsuda
,
A.
, and
Kojic
,
M.
,
2006
, “
An Implicit Algorithm Within the Arbitrary Lagrangian-Eulerian Formulation for Solving Incompressible Fluid Flow With Large Boundary Motions
,”
Comp. Methods Appl. Mech. Eng.
,
195
, pp.
6347
6361
.10.1016/j.cma.2005.12.009
35.
Haber
,
S.
,
Yitzhak
,
D.
, and
Tsuda
,
A.
,
2003
, “
Gravitational Deposition in a Rhythmically Expanding and Contracting Alveolus
,”
J. Appl. Physiol.
,
95
, pp.
657
671
.
36.
Pedley
,
T. J.
,
Schroter
,
R. C.
, and
Sudlow
,
M. F.
,
1977
, “
Gas Flow and Mixing in the Airways
,” in
Bioengineering Aspects of the Lung
, edited by
J. B.
West
,
Marcel Dekker
,
New York
.
37.
Weibel
,
E. R.
,
Sapoval
,
B.
, and
Filoche
,
M.
,
2005
, “
Design of Peripheral Airways for Efficient Gas Exchange
,”
Respir. Physiol. Neurobiol.
,
148
(
1–2
), pp.
3
21
.10.1016/j.resp.2005.03.005
38.
Weibel
,
E. R.
,
1963
,
Morphometry of the Human Lung
,
Springer/Academic
,
Heidelberg
.
39.
White
,
F. M.
,
1974
,
Viscous Fluid Flow
,
McGraw-Hill
,
New York
.
40.
Pozrikidis
,
C.
,
1994
, “
Shear Flow Over a Plane Wall With an Axisymmetric Cavity or a Circular Orifice of Finite Thickness
,”
Phys. Fluids
,
6
, pp.
68
79
.10.1063/1.868046
41.
Haber
,
S.
,
Yitzhak
,
D.
, and
Tsuda
,
A.
,
2010
, “
Trajectories and Deposition Sites of Spherical Particles Moving Inside Rhythmically Expanding Alveoli Under Gravity-Free Conditions
,”
J. Aerosol. Med. Pulm. Drug Deliv.
,
23
(
6
), pp.
405
413
.10.1089/jamp.2009.0774
42.
Semmler-Behnke
,
M.
,
Kreyling
,
W. G.
,
Schulz
,
H.
,
Takenaka
,
S.
,
Butler
,
J. P.
,
Henry
,
F. S.
, and
Tsuda
,
A.
,
2012
, “
Nanoparticle Delivery in Infant Lungs
,”
Proc. Natl. Acad. Sci. U.S.A.
,
109
(
13
), pp.
5092
5097
.10.1073/pnas.1119339109
You do not currently have access to this content.