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Saint Louis University School of Medicine, Department of Pediatrics at Cardinal Glennon Children's Hospital, and Saint Louis University Department of Mathematics, Saint Louis, Missouri 63104
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Albers, G. M., R. P. Tomkiewicz, M. K. May, O. E. Ramirez,
and B. K. Rubin. Ring distraction technique for measuring surface
tension of sputum: relationship to sputum clearability. J. Appl. Physiol. 81(6):
2690-2695, 1996.
Poor sputum clearance has been related to sputum
adhesion tension. In this study, we describe a modified du Noüy
ring method for measuring the surface tension (
) of small samples of
sputum and for comparinge the calculated work of adhesion
(Wad) for sputum specimens with
the measured mucociliary transportability (MCTR) and cough
transportability (CTR). The , as measured by this method, correlates
with measured by sputum contact angle on a low-surface-energy solid
(R2 = 0.368, P = 0.03). There is a small
but significant difference in measurements made by these two methods
(P = 0.03).
Wad calculated from the surface
tension ring method is inversely correlated with CTR
(R2 = 0.181, P = 0.004) but has no
correlation with MCTR in this study. The miniaturized ring method gives
accurate and reproducible measurements of the surface tension of small
amounts of respiratory secretions. Because sputum behaves enough like a
liquid that the assumptions made in using the Young equation to
calculate Wad appear valid, we
also showed that the Neumann equation can be used to determine the
surface tension of sputum by its contact angle on tetrafluoroethylene
(Teflon).
physical properties of sputum; adhesion; surface properties; cystic
fibrosis; chronic bronchitis
INTRODUCTION RESPIRATORY MUCUS is a viscoelastic gel that is
secreted into the airways and spreads over the surface of the airway
epithelium in contact with the tips of the cilia and the periciliary
fluid layer (12, 18, 20). Normally, mucus is cleared to the proximal airway by the direct interaction of beating cilia with the surface of
the mucus. When there is hypersecretion or ciliary damage, secretions
are cleared by cough, which is dependent on the flow of air to remove
the mucus accumulated in the airway (10). In both of these forms of
clearance, the physical properties of mucus play a role. These
properties include viscoelasticity as well as surface interactions as
mucus forms an interface with the underlying epithelium. Work must be
done to overcome the forces that are active at the mucus-epithelium
interface. The work required to separate 1 cm2 of an interface between two
substances is called the work of adhesion
(Wad)
The gellike properties of mucus make determinations of surface tension
difficult. At least two methods for measuring the surface tension of
sputum have been reported. Puchelle and colleagues (15) described use
of the du Noüy ring distraction method to directly measure
surface tension The rationale for conducting these studies was to develop a simple,
reproducible method to evaluate the surface properties of airway
secretions so that the role these characteristics play in airway
clearance can be studied. The purpose of this study was twofold. First,
we wanted to validate the use of a small platinum-iridium ring for
determining the surface tension of small samples of sputum by comparing
these measurements to values calculated from the contact angles of the
same samples on a low-surface-energy solid. We also assessed the
relationship between the Wad for a
sputum-glass interface to the measured mucociliary transportability
(MCTR) and cough transportability (CTR) of the sputum samples. This was done to evaluate the role that surface properties have on the transportability of airway secretions by using a variety of specimens from patients with chest disease.
METHODS Sputum samples were obtained by expectoration from patients with cystic
fibrosis (CF) lung disease and chronic bronchitis (CB) who were not
currently experiencing an exacerbation of their disease. The patients
were asked to swallow all saliva before expectoration, and then the
sputum was separated from any remaining saliva before
conducting our analyses. Specimens were stored at
where
(1)
1 is the surface tension of one
substance at an interface, 2 is
that of the other substance, and
1, 2 is the interfacial tension between the two (1). When a liquid rests on the surface of a
solid, in most instances the liquid will not completely wet the solid
and will form a drop on the surface with a discrete contact angle
(
). When this system is at equilibrium, Young's equation
(Eq. 2) applies, where
lv is the interfacial tension between the liquid phase and its vapor,
sv is the interfacial tension
between the solid and vapor, sl
is the interfacial tension between the solid and the liquid, and is
the discrete contact angle that the liquid forms on the solid (Fig.
1)
Equations
1 and 2 can be
combined to give
(2)
To
calculate Wad for a mucus-surface
interface from Eq. 1, we must be able
to measure the surface tension of the mucus, the surface tension of the
surface on which the mucus is resting, and the interfacial tension
between the two. However, if we assume that mucus behaves enough like a
liquid to accept the Young equation, we can calculate the
Wad for a particular mucus
interface by using Eq. 3, in which we
only need to measure the surface tension of the mucus and its contact
angle on the surface in question.
(3)
Fig. 1.
Diagram of a 3-phase system [vapor (v), liquid (l), solid
(s)] demonstrating contact angle (), surface tension solid
(sv), surface tension liquid
(lv), and interfacial tension
between solid and liquid
(sl). TFE,
tetrafluoroethylene.
[View Larger Version of this Image (9K GIF file)]
ring, using a standard ring, 10-mm in
diameter and 0.7-mm thickness. This technique is limited by the
relatively large amount of sputum (250 µl) needed for the measurement. Smaller samples can be used in a second method described by Pillai et al. (14), which treats mucus as a solid and calculates from the contact angle formed on the sputum by a liquid with known
surface tension (glycerol). This approach is based on an equation-of-state relationship described by Neumann et al.
(13) and Pillai et al. (14) to determine the surface
tensions of low-energy solids by contact angles. Neither method of
determining the surface tension of mucus has been validated against the
other, in part because of the difficulties in evaluating the surface tension of a gel.
70°C until
analysis. None of the CF patients had been treated with recombinant
human deoxyribonuclease or were using any mucoactive medication.
Approval to collect and use sputum from patients for in vitro analysis
was obtained from the St. Louis University School of Medicine
Institutional Review Board.
= 72.8 dyn/cm. The small-ring calibration was then checked against water.
Values were read from the tensiometer and were corrected for the
difference in size of the ring (the circumference of the small ring is
3.8 times less than the standard ring).
of all sputum samples were also measured on acid-washed,
ethanol-dried glass slides (
glass). A random subset of
samples was chosen for measurement on tetrafluoroethylene (TFE, or
Teflon) as well. These same sputum samples had surface tension
calculated with the use of the Neumann equation from their advancing
on TFE, a low-energy solid with a surface tension of 18 dyn/cm (13, 14). In both instances, analysis was done with a sample volume of 30 µl in 100% relative humidity by a modification of a previously described image analysis technique (5, 19).
The of a series of liquids with known surface tension were measured
on glass by the same method to generate a best-regresson fit of on
glass against known surface tension. The liquids were chosen because
their surface tensions spanned a range of 21.97 to 63.4 dyn/cm (ethanol
to glycerol, respectively; 11). These measurements were made in the
same chamber as the sputum samples but without additional
humidification. The temperature of the chamber was 25 ± 1°C.
MCTR.
MCTR was measured by using the frog palate technique (16, 17). Palates
isolated from frogs (Rana pipiens),
spontaneously depleted of native mucus but still cilioactive, were
placed in a Plexiglas chamber controlled for temperature (25°C) and
100% relative humidity. Samples ~2 µl in volume were placed on the palate, and the trailing edge velocity was computed from the transit time over a 5-mm path at the midline of the palate. On the average, three to eight measurements were taken for each sample to calculate a
mean velocity. To take into account the variability of transport rates
on the palates, the values were standardized by expressing them as the
ratio of the mean sample velocity over the mean velocity of native frog
mucus before and after the human sample on the same palate. This
normalized ciliary transportability rate is presented as MCTR.
CTR.
CTR of the samples was measured in a simulated cough machine with
constriction (2). The cough machine is a Plexiglas model trachea
connected to an 8-liter tank containing air pressurized to 6 pounds/inch2 (psi). A solenoid
valve controls air release through a flow-constrictive element used to
mimic the airflow pattern of a natural cough. A sinusoidal constriction
(length 7.7 cm, height 8 mm) is used to decrease the airway diameter,
while minimizing the turbulence of the system for a small airway model.
The peak linear air velocity is ~120 m/s, with the 4-mm gap at a flow
rate of 11 liters/s. A sample of ~30 µl is spread in a thin line of
~0.5-mm depth across the base of the trachea. The distance traveled
by the sputum under the effect of the airflow, measured in millimeters,
is presented as CTR.
Statistical analysis and graphing calculations.
The graphs for Eq. 4 were produced
with the use of either Maple V5.3, Waterloo Maple Software, or
Differential Systems 3.0, Drexel University (1991) on an Apple Power PC
7100. The Neumann equation was simplified, and computations were done
using xFunctions 2.2, written by David Eck with support from National
Science Foundation Grant USE-905158313 (13, 14). Statistical analysis
was performed using the StatView 4.1 statistics package (Abacus
Concepts, Berkeley, CA). Results of the analyses are reported as means ± SD. Equality of means was tested by the analysis of variance
(ANOVA), and association between characteristics was tested by
regression analyses. In all cases, P 
0.05 was considered significant.
RESULTS
Surface tension values measured by the ring method are reported for all
CF and CB samples, and surface tensions measured by the contact angle
method are reported for a subset of these in Table
1. There is a significant correlation
between values determined by the two methods (Fig.
2, R2 = 0.368, P = 0.03), although there is
a difference between surface tension measurements by the two methods
(P = 0.03), with the values by
contact-angle method usually being higher when is <90 dyn/cm. We
also report in Table 1 the measured contact angles on glass that are
used to calculate Wad-glass by
Eq. 3, as well as the contact angles
measured on TFE that were used to calculate -contact angle by
Eq. 4.
Wad was calculated from
Eq. 3 using calculated by either
the ring method or the contact angle method. So that both calculations
of Wad described the same
interface (sputum-glass), the contact angle on glass was chosen to
represent .
|
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) of sputum measured by its on TFE (or Teflon)
plotted against measured by ring method. CF, cystic fibrosis; CB,
chronic bronchitis. There is a significant correlation between measured by 2 methods;
R2 = 0.368, P = 0.03. Shaded line
represents line of identity.
In Fig. 3, the mean values ± SD of
glass and
ring of CF and CB sputum were
superimposed onto a regression curve made from the contact angles
measured on glass of a series of liquids plotted against their known
surface tension (8). This was done to demonstrate the close
relationship to the tail of the regression curve that ring for these sputum samples have.
on glass
(glass) compared with (dyn/cm) for series of liquids with known surface tension. Mean ± SD of by ring method and
glass of CF and CB sputum are
superimposed on this curve displaying their relative positions. Dotted
portion of line represents extrapolation of curve past measured known liquids.
The MCTR and CTR of samples of sputum were measured and compared with
Wad on glass to describe the
relationship between the surface properties and the ability to clear
these secretions from the airway. A significant inverse correlation
between Wad and CTR
(R2 = 0.181, P = 0.004) is shown in Fig.
4. However, there was no correlation
between Wad and MCTR, as seen in
Fig. 5.
DISCUSSION
This study was undertaken to develop a simple, reproducible method for
measuring the surface tension of small samples of mucus or sputum. The
method reported here is a modification of the ring technique described
by Puchelle et al. (15). Although Puchelle's du Noüy ring method
requires a sample size of 250 µl, we have been able to accurately
measure in samples of sputum as small as 30 µl by using this
smaller ring. The values for Wad
for CF and CB sputum, shown in Table 1, are very similar to those
reported by Girod et al. (6, 7). In the report of Puchelle et al., was measured for CF sputum and known liquids with the ring, and a
decrease in measured surface tension was demonstrated after adding
sodium dodecyl sulfate, a surface tension-lowering agent, to the
sputum. We have shown that the small ring accurately and reproducibly
can measure and that these values are consistent with surface
tension measurements calculated from the contact angle measured on TFE.
The ring method appears to give accurate surface tension measurements
of sputum in that the two methods arrive at values in the same range.
However, the miniaturized ring technique gives sputum surface tension
values that are usually lower than those calculated from contact
angles, except, it appears, when there are much higher surface
tensions. This may in part be due to the effect of cohesion which could
contribute to the apparent surface tension by the sample stretching
before release from the ring. Precision of measurements will remain an
issue because of the heterogeneity of the samples.
Mucus or sputum is a non-Newtonian liquid, so that with spreading on a
surface, some energy may be stored as the elastic modulus. Therefore
the contact angle may not truly represent the change in energy that
occurred to increase the surface as the mucus spread to form the
interface. When the Young relationship is used to describe mucus
surface properties, the liquidlike behavior of mucus is assumed. This
can introduce some error; specifically, if a sample of mucus does not
spread completely, surface tension will tend to be underestimated, but
relative changes in surface tension will be evaluable. Further, the
significant but rather small difference between measured by the
ring method, which does not depend directly on the liquid behavior of
mucus, and measured by contact angles, also suggests that any error
in assuming liquid behavior is small as well.
An alternative method for evaluating the surface tension of mucus or sputum is to assume that the sputum behaves much like a solid and then to evaluate the spreading of an ideal liquid placed on the mucus layer by using the Neumann equation of state of approach, as used by Pillai and colleagues (14). To understand the limitations that the Neumann equation-of-state approach (Eq. 4) imposes on measuring surface tension, we graphically solved Eq. 4 as shown in Fig. 6 (13)
![cos&thgr; = <FR><NU>(0.015 &ggr;<SUB>sv</SUB> − 2.00)(&ggr;<SUB>sv</SUB>&ggr;<SUB>lv</SUB>)<SUP>½</SUP> + &ggr;<SUB>lv</SUB></NU><DE>&ggr;<SUB>lv</SUB>[0.015(&ggr;<SUB>sv</SUB>&ggr;<SUB>lv</SUB>)<SUP>½</SUP> − 1]</DE></FR>](/content/vol81/issue6/fulltext/2690/img004.gif)
|
(4) |
lv (surface tension of the
liquid drop) and sv (surface
tension of the solid surface) that give a constant value for cos()
were plotted. It is apparent that a given
lv cannot solve for a
sv that is equal to or greater than itself. This is demonstrated in the figure as the line where cos() = 1. This makes physical sense in that when cos()
approaches 1, the contact angle approaches 0, and the liquid has
completely wetted the solid. The range of evaluable solid-surface
tensions can be broadened by use of the complementary angle when
evaluating surfaces other than very-low-surface energy solids, but to
use this method to measure the surface tension of a "solid", the
liquid chosen must have a surface tension above the possible range
suspected for the solid. If we use the equation differently, using a
very low-energy surface such as TFE
(sv = 18 dyn/cm) as the known, and solve for an unknown lv, in
the graphic solution there are valid solutions in an approximate range
of lv from 18 to 110 dyn/cm
(Fig. 6). A sv of 80 dyn/cm or
greater, can only be solved outside the triangular
region on the graph described by the plots of cos() = 1 and
cos() = 1, where the equation makes sense. This demonstrates that
treating mucus as the liquid phase and TFE as the solid phase allows us
the widest range in which to evaluate the surface tension of mucus, and
this is the only valid use of the state-of-approach equation in this
situation.
lv vs.
sv with cos plotted in
regions where values are constant. Shaded triangular region between
cos = 1 and cos = 1 is where cos remains constant and
equation is solvable. Line cos = 1 is line of identity, where
lv = sv. At this point, has
approached 0, and surface is completely wetted. It is impossible to
solve for sv > lv.
After mathematical verification that the Neumann state-of-approach
equation could solve for higher surface tensions when a true low-energy
solid was used to calculate , we showed that this method could be
used to calculate the surface tension of mucus as well. Using this
method is most consistent with the basic assumption in the Neumann
equation that the solid is a low energy, homogeneous, nondeformable
surface.
We demonstrated that the relationship of contact angle to surface tension holds on glass surfaces, as used by Puchelle and colleagues (15) as well. However, because acid-washed, ethanol-dried glass slides are wettable and are not low energy solids, they cannot be used in the same way as TFE to derive surface tension. We used a series of liquids with known surface tensions to demonstrate the association between contact angle on glass of those liquids with their known surface tensions. The close relationship that our values for sputum had to the regression curve for this series of pure liquids further demonstrates that, for purposes of surface measurements, it is safe to assume that sputum behaves much like a Newtonian liquid. If the contact angle is measured on this glass surface, it is possible to use Fig. 3 to extrapolate surface tension.
An attempt was made to compare the ring method directly to the
technique described by Pillai et al. (14). When there was a large
difference in the values noted between the two methods in a pilot study
(not reported here), the mathematical assumptions of the Neumann
state-of-approach equation (13) were reviewed. It was noted that, when
performing measurements as described by Pillai et al., if the surface
energy of the "solid" (mucus) is equal to or greater than the
test liquid (glycerol), the equations solve to an invalid answer. The
surface tension for CF sputum was determined by the ring method to be
81.1 ± 3.36 dyn/cm. Therefore, when using glycerol with a of
63.4 dyn/cm, it is not possible to measure sputum surface tension.
Furthermore, this technique, although using advancing contact angles to
minimize the effect of heterogeneity and deformability of the mucus
surface, makes the assumption that glycerol is chemically inert in
regards to the mucus. Glycerol, however, is miscible with water and
actually absorbs water from the air (3). We attempted to reproduce this technique, using mercury as a nonmiscible liquid with surface energy
significantly higher than the possible values for mucus ( = 485.48 dyn/cm at 25°C), but the surface of the mucus readily deformed,
invalidating the assumption that the mucus would behave like a solid.
We also demonstrated that the surface properties of mucus affect its transportability. The Wad of sputum inversely correlates with the ability to clear these secretions as assayed by a simulated cough. This correlation has been previously reported by King and colleagues (11) and is logical, as cough must separate the mucus-epithelial interface to propel the mucus forward. The lack of a correlation between Wad and MCTR may be due to a more complex dependency of mucociliary clearability on other rheologic characteristics, especially viscoelasticity (4, 9).
Wad is a characteristic of two substances, each with unique surface tensions, that share an interface. It is the work that is done to overcome the interfacial tension and effect a separation of these two substances. When describing the Wad for respiratory secretions, we must specify the interface that is being evaluated, i.e., mucus-glass, mucus-TFE. The ideal would be to describe the mucus-epithelium interface. Differences in the interface may arise in either component of the system. Just as mucus specimens have different surface characteristics, so do the surfaces we measure them on. Differences in the Wad of a particular interface may better reflect the differences in the surface than the mucus. For example, acid washing renders the surface of slides negatively charged; differences in Wad between specimens calculated from these surfaces may be influenced by covalent forces that do not apply at an epithelial surface. This points out the need to develop further ways of studying mucus as part of a mucus-epithelium system in which the unique characteristics of each component lead to a unique interaction.
ACKNOWLEDGEMENTS
The authors thank Dr. Samuel Schürch, University of Calgary, Alberta, Canada, for helpful comments in the development of this study and Jayson Clark of St. Louis University for help with mathematical computations and acknowledge the expert technical assistance of Titik Dian.
FOOTNOTES
Address for reprint requests: B. K. Rubin, Prof. of Pediatrics, Saint Louis Univ. School of Medicine, 1465 S. Grand Blvd., Saint Louis, MO 63104-1095 (E-mail: RUBINBK{at}SLUVCA.SLU.EDU).
Received 29 February 1996; accepted in final form 7 August 1996.
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