Respiratory Physiology & Neurobiology 150 (2006) 261277

In vivo measurements of human oral cavity heat and

water vapor transport
J.W. Kaufman
a,
, K. Farahmand
b
a
Naval Air Warfare Center Aircraft Division, Human Performance Technology Branch, Code 4656, Bldg 2187 Suite 2280,
48110 Shaw Rd. Unit 5, Patuxent River, MD 20670-1906, USA
b
Department of Mechanical and Industrial Engineering, Texas A&M University-Kingsville, Kingsville, TX 78363, USA
Accepted 17 May 2005
Abstract
Oral heat and water vapor transport may play a signicant role in maintaining airway health. This study intended to develop
a technique for measuring heat and mass transfer coefcients in the human oral cavity as a function of ow rate. A multi-
thermocouple probe was developed which simultaneously measures dry and wet bulb temperatures at two airstream sites while
also measuring three buccal wall temperatures. Oral temperature data (airstream and buccal surface) were acquired from eight
subjects (two females and six males) breathing at varying ow rates to calculate transport coefcients. Techniques used to
validate probe accuracy included correlating experimentally measured heat transfer in a smooth pipe with theoretical plug ow
in a circular conduit. Experimental results suggest that modeling the oral cavity as a circular conduit is problematic because Nu
measured in a heated pipe differs so greatly from Nu measured in the oral cavity.
Published by Elsevier B.V.
Keywords: Respiration; Heat exchange; Mass transfer; Mechanics of breathing
1. Introduction
The path inspired air traverses in the upper airway
plays an important role in maintaining health as
evidence suggests that rapid oral breathing contributes
signicantly to the onset of cold-induced asthma. Deal
et al. (1979) demonstrated that oral inspiration of cold
air can elicit bronchospasms. This probably results

Corresponding author. Tel.: +1 301 342 8883;

fax: +1 301 342 8876.
E-mail address: jonathan.kaufman@navy.mil (J.W. Kaufman).
from convective or evaporative cooling of bronchial
smooth muscle during oral breathing (Souhrada et al.,
1983), which McFadden and Pichurko (1985) found
to occur at elevated minute ventilations. Presumably,
increasing airow prevents inspired air from being
adequately warmed and humidied within the oral
cavity and passes the conditioning burden to the lower
airways.
Normally, this is not a problem because most rest-
ing humans breath nasally. The nose has been shown
to be extremely efcient in warming and humidifying
inspired air (Kaufman, 1993; Webb, 1951) but less is
1569-9048/$ see front matter. Published by Elsevier B.V.
doi:10.1016/j.resp.2005.05.016
262 J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277
known about the efciency of the oral cavity in these
tasks. This becomes an issue when minute ventilation
exceeds roughly 30 Lmin
1
because oronasal breath-
ing commences (Niinimaa et al., 1981). If the oral
cavity is less efcient than the nasal cavity at condi-
tioning inspired air then cold air may pass into thoracic
airways and produce bronchospasms. Assessing oral
cavity efciency in conditioning inspired air is difcult,
however, because it is unclear how to model oral heat
and water vapor exchange at normal and elevated ven-
tilation rates given the complex anatomical geometry.
In addition, nasal breathing efciently removes
airborne particles (>1 m diameter) before they reach
the respiratory airways (Larson, 1989). Deposition
plays a major role in removing inspired airborne
particles and depends on particle mass as dened by
the mass median aerodynamic diameter (MMAD). For
hygroscopic particles, MMAD depends on initial par-
ticle size and particle growth due to hydration. Rapid
increases in nasal airstream relative humidity promote
rapid particle growth and subsequent nasopharyngeal
deposition. Particle growth and deposition during oral
breathing is less clear because oral cavity humidity
proles are unknown.
Numerical models can be used to predict respiratory
tract temperature proles and intra-airway hygroscopic
particle growth, but to do so they require knowledge
of oral cavity humidity proles. Respiratory water
exchange is coupled to heat exchange, so both must
be quantied for reliable modeling. Calculating oral
heat and water vapor exchange requires both airstream
and surface temperature and airstream humidity data.
In addition, oral cavity geometry and ow rate must be
dened at the time of temperature measurements.
Hersh et al. (1943) were among the rst to attempt
to characterize oral cavity surface temperatures, though
no attempt was made to measure oral airstreamtemper-
atures. McCutchan and Taylor (1950) and Proctor and
Swift (1977) measured airstream temperatures at the
lips and pharynx and Primiano et al. (1988) also mea-
sured surface temperatures at these sites. Eisner and
Martonen (1989), Ingenito et al. (1987), and Primiano
et al. (1984) each developed systems to simultaneously
measure oral temperatures. These probes, however,
either measured airstream and surface temperatures or
airstream temperature and humidity at a single point.
Calculating heat transfer coefcients requires sequen-
tial measurements at different surface sites.
The purpose of this study was to develop a probe that
can be used to study human oral cavity heat and water
vapor exchange by simultaneously measuring multiple
site humidities and temperatures during normal and
elevated respiration. This approach minimizes mea-
surement errors associated with dynamic changes in
oral cavity morphology and surface blood ows change
during respiration. Oral heat and water vapor exchange
rates, in the formof heat and mass transfer coefcients,
can then be calculated from humidities and temper-
atures measured in the human oral cavity. Numerical
models using these experimental heat and mass transfer
coefcients, combined with related studies elucidating
lower airway transport coefcients, can then be used
to explore the etiology of cold-induced asthma and to
predict factors inuencing particle deposition.
2. Methods
2.1. Physical design
Oral cavity heat and mass transfer coefcients
represent heat and water vapor exchange rates between
the airstream and internal surfaces (buccal surface,
tongue, and hard palate). Calculating heat transfer
coefcients depends on dening an airstream con-
trol volume, measuring inlet and outlet airstream
temperatures, volumetric ow rate, and surfaces
temperatures at the locations corresponding to the
airstream temperature measurements (Fig. 1) (Bird et
Fig. 1. Schematic drawing depicting the variables needed for calcu-
lating heat and mass transfer between an airstream and surface in a
circular conduit. An airstream control volume is bounded by dotted
lines 1 and 2, representing inlet and outlet planes, respectively. Sym-
bols shown are: L and D, control volume length and diameter; V
E
,
minute ventilation;
a
, air density; T
a
and T
s
, airstream and surface
temperatures; C
a
and C
s
, airstream and surface temperatures.
J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277 263
al., 1960). Determining water vapor exchange rates
is analogous to calculating heat transfer, except that
airstream and air/surface interfacial humidity, rather
than temperature, must be determined.
Characterizing oral cavity heat and water vapor
exchange is plagued by problems associated with
dynamic changes in oral passage morphology and
surface blood ows. Normal oral breathing entails
near-instantaneous changes in buccal blood ow
caused by changing oral heat exchange. Accelera-
tion/deceleration of the chest wall throughout the
breathing cycle produces unsteady oral air ows which,
combined with varying oral geometry (caused by
changing tongue and buccal surface positions), alter
buccal surface heat exchange andthe subsequent vascu-
lar responses. As a result, any experimentally measured
heat and mass transfer coefcients represent only the
conditions dened at the time of measurement.
One way to surmount (or at least minimize) this
problem is to simultaneously obtain all of the data
required to calculate oral heat and water vapor transfer.
To do this, a probe was developed which measures
multiple airstream and surface temperatures simulta-
neously while allowing unimpeded, though disturbed,
airow (Figs. 2 and 3). This approach minimizes the
time required to capture oral cavity data, reducing (but
not eliminating) the effects of constantly changing
oral conditions. Seven 0.005 cm diameter (44 AWG)
type T thermocouples were mounted near the tip of
a sealed 17.6 cm long Tygon tube (R-3603, 0.16 cm
i.d. and 0.48 cm o.d.). Thermocouples were calibrated
at 0

C (stirred ice bath) and 29.772

C (Yellow
Springs Instruments, Yellow Springs, OH, model
17402 Gallium Temperature Standard). Airstream
temperatures were measured by two dry bulb (DBT2
and DBT4) and two wet bulb (WBT2 and WBT4)
thermocouples that allowed humidity and temperature
to be simultaneously determined at two separate points
in the airstream. Relative humidity was computed
psychrometrically. Precisely measuring surfaces tem-
peratures corresponding to each pair of dry and wet
bulb thermocouples was impossible because adjacent
dry and wet bulb thermocouples were not exactly
the same distance along the probe and their position
shifted slightly with use. To compensate, surface
temperatures were measured at three points (DBT1,
DBT3, and DBT5) that bracketed the positions of
the airstream thermocouples. Surface temperatures
Fig. 2. Schematic drawing depicting the oral cavity temperature probe used in this study. Dry and wet bulb thermocouples are indicated by DBT#
and WBT#. Wire guards constructed of 24 AWG steel wire protect thermocouples from bending or rough handling while allowing unobstructed
thermocouple contact with the buccal surface and exposure to the airstream. (A) The probe longitudinally and (B) a radial view.
264 J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277
Fig. 3. Oral cavity temperature probe prior to placing it inside the oral cavity.
were dened as the average of the two thermocouples
bracketing the position of the airstream pair.
2.2. Thermocouple response time
Characterizing expiratory or inspiratory tempera-
ture curves during normal breathing requires at least
three temperature measurements per expiratory or
inspiratory phase. To obtain accurate measurements,
the thermocouple response time, , which is dened as
the time to reach 63.2% of a temperature step change,
must be minimized. The minimum was calculated by
assuming a breathing frequency of 16 breaths min
1
and a 500 mLtidal volume. Since this breathing pattern
produces single breaths (inspiration and expiration)
lasting 3.75 s, if one assumes equal inspiratory (t
I
)
and expiratory (t
E
) times of 1.875 s each expiratory
or inspiratory temperature sampling period would last
0.625 s. As 5 is necessary to achieve a stable 100%
step change value (Omega, 1989), a <0.125 s is
required to accurately determine three expiratory or
inspiratory temperatures per breath.
The technique of Farahmand and Kaufman (2001)
was used to measured dry bulb thermocouple . The
thermocouple was placed between two rapid response
(response time <15 ms) solenoid valves controlling air-
ows at different temperatures. Energizing the valves
sequentially produced approximated temperature step
changes. The temperature response was measured with
a signal conditioner (AnalogDevices, 3Bseries, model:
3B47-T-07) and computer (Dell Systems, windows
operating system) and the time to reach 63.2% of the
ambient dry bulb temperature calculated. Using this
technique, dry bulb thermocouple response time was
55 4 ms at air velocities =3.13.7 ms
1
.
A related technique was used to quantify the wet
bulb thermocouple response time (Kaufman et al.,
2004). The experimental conditions were selected to
simulate human respiratory conditions. The apparatus
produced repeatable square waves and allowed change
in direction of temperature gradient without difculty.
The experiment was carried out for both cooling
(going from hot to cold) and heating (going from
cold to hot) of the thermocouple using two different
housing dimensions of 2.54 and 3.33 cm.
Conduction along thermocouple wire and radiation
effects was shown to negligibly affect response times.
The effects of small incremental temperature changes
and temperature gradient direction were also found
to be insignicant. There was also no correlation
between air velocity and response time of wet bulb
thermocouple (Kaufman et al., 2004) though a positive
correlation between air velocity and response time
of a dry bulb thermocouple has been demonstrated
J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277 265
(Farahmand and Kaufman, 2001). Wet bulb thermo-
couple response time was 175.0 63.9 ms (2.54 cm
housing) and 152.5 50.3 ms (3.33 cm housing) at air
velocities =1.52.5 ms
1
.
Reducing minimizes temperature measurement
error by minimizing the difference between measured,
T
meas
, and actual, T, temperature changes during
sinusoidal temperature oscillations, since
T
meas
T
=
1
_
1 +()
2
(1)
where is the angular frequency (Michalski et
al., 1991). Assuming a maximum breathing rate of
50 breaths min
1
, T is underestimated a maximum
of 3% in dry bulb measurements and 11% with wet
bulb thermometry. Temperature measurement error,
e
m
, associated with actual temperature rate of change
(dT/dt),

T
ac
, can also be estimated from . Modeling
airstream temperature change as a ramp function, the
relationship between e
m
and is given by
e
m
=

T
ac
exp
_
t

_
+

T
ac

C (2)
where the terms on the right side of the equation are
the transient and steady state error terms, respectively
(Doebelin, 1975). The effect of increasing t on T
(%) can be seen in Fig. 4 for

T
ac
=22.4

Cs
1
, the
Fig. 4. Temperature measurement error due to differences in ther-
mocouple response time, , as a function of sampling time when the
temperature rate of change =22.4

Cs
1
. Note that error increases
for both the transient and steady state portions of each curve as
increases.
temperature rate of change observed in this study
corrected for . Since

T
ac
will be less than 22.4

Cs
1
except under extreme conditions, e
m
will be <5%
for both DBT and WBT measurements. Farahmand
and Kaufman (2001) used an energy balance between
convective heat transfer and heat accumulation in the
tip for this ideal system which is given by
hA(T
amb
T
tc
) = mc
dT
tc
dt
(3)
where h is the lm convective heat transfer coefcient,
A the thermocouple tip surface area, T
amb
the ambient
environmental temperature, and T
tc
, m, and c represent
the temperature, mass, and heat capacity of the
thermocouple tip, respectively. The time constant, ,
is then dened as
=
cV
hA
(4)
Thermocouple response to an ambient temperature step
change from T
amb,1
to T
amb,2
can then be described by
T
tc
= T
amb,1
+(T
amb,1
T
amb,2
) e
t/
(5)
Graphical solutions were used to quantify from
experimental data. The initial thermocouple transient
period was identied from the log linear portion of the
response curve. Transforming temperature data as
log T =

1
T
f
T

(6)
where T is the thermocouple temperature and T
f
is the nal recorded thermocouple temperature,
the temperature curve initially displays non-linear
behavior followed by a rst-order (linear) response.
The initial non-linear part of the logarithmic curve
represents transient responses resulting from moving
the thermocouple from one conduit to another. The
initial non-linear temperature response regions were
omitted when calculating thermocouple response
times. First-order linear regression was used to
t a line through the inection point marking the
exponential (log linear) portion of the curve. The time
constants for the wet bulb was characterized by
=
m
eff
c
eff
h
eff
A
(7)
The m
eff
and the c
eff
could be obtained by com-
bining the mass and specic heat for water and the
266 J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277
Fig. 5. Schematic drawing of the system used to verify that the temperature probe could accurately determine heat transfer in a closed conduit.
Probe position within the pipe closely approximated its position within the human oral cavity during in vivo measurements.
thermocouple bead.
m
eff
c
eff
= m
w
c
w
+m
b
c
b
(8)
The effective heat transfer coefcient is given by
h
eff
= h
D

w
c
p
_
Sc
Pr
_
2/3
(9)
where h
D
=f/2,
w
and c
p
are the density and specic
heat of water, Sc the Schmidt umber, Pr the Prandtl
number, and f is the friction factor for ow of air over
a lm of water (drag coefcient) which is a constant
0.5, for Reynolds number ranging from 10
3
to 10
5
(White, 1991).
2.3. Pipe ow measurements
Unidirectional airow was modeled in a straight
pipe in order to estimate the role of oral cavity mor-
phology on heat and water vapor transport. Fig. 5 shows
the equipment used for these measurements. The tem-
perature probe was positioned along the lower pipe
surface with the most proximal thermocouple 3.1 cm
fromthe inlet. Pipe wall temperature was maintained at
40

C and ow rate was varied from 0.3 to 50 Lmin

1
.
Temperature measurements were taken after a constant
airow was maintained for 5 min. Three sets of 5-min
readings were obtained at each ow rate.
2.4. Oral temperature measurements
Eight non-smoking adults (two females and six
males) without histories of chronic respiratory disease
or evidence of oral disease were studied after being
fully informed of the benets and risks of this study.
Each subject performed standard spirometry tests
(Ventilation Measurement Module, model VMM-2,
Sensormedics, Anaheim, CA) to determine their rest-
ing tidal volume (V
T
), forced vital capacity (FVC), and
forced expiratory ow in 1 s (FEV
1.0
). The following
oral cavity dimensions were also measured: (a) width
of closed lips at widest point, (b) oral cavity length
from lips to pharyngeal wall, (c) distance from upper
to lower lip with fully opened mouth, (d) width of
opened lips at widest point with fully opened mouth,
and (e) distance from upper tongue surface to hard
palate with fully opened mouth. Table 1 summarizes
these anatomical and physiological results.
Expiratory and inspiratory oral temperature mea-
surements were obtained after a seated subject placed
the temperature probe along their right buccal surface
with the probe tip 7.0 cm from the lips. This placed the
most proximal thermocouple, DBT5, approximately
2.5 cm from the lips. Airstream thermocouples were
approximately 21 1 cm above the lingual surface
during measurements due to compression of the
lingual thermocouples (Fig. 2). This distance is less
J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277 267
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than half the oral cavity height in all but two subjects
(Table 1), so airstream thermocouples were generally
further from the palate than the lingual surface during
measurements. Assuming oral laminar ow, DBT2 and
WBT2 lay outside the lingual thermal boundary layer
at Re >282 and DBT4 and WBT4 at Re >196. Con-
sequently, airstream thermocouples were outside the
thermal boundary layer for nearly all measured ow
rates.
A nose clamp was used to compel subjects to
breath only orally. The same breathing sequence was
employed in all trials and data was continuously
collected until after the breath hold period. Initially,
subjects breathed quietly (V
T
=649 154 ml, breath-
ing frequency (f) =17.3 2.8 breaths min
1
(bpm),
and minute ventilation (V
E
) =11.2 Lmin
1
) for
2 min. This was immediately followed by a series
(1 min each) of deep slow (V
T
=1924 397 ml,
f =9.0 3.0 bpm, and V
E
=17.3 Lmin
1
), nor-
mal (V
T
=1545 393 ml, f =12.4 3.4 bpm, and
V
E
=19.2 Lmin
1
), and rapid (V
T
=1543 332 ml,
f =16.8 4.0 bpm, and V
E
=25.9 Lmin
1
) breathing.
Subjects were then directed to take shallow breaths at
a normal (V
T
=538 182 ml, f =19.0 4.7 bpm, and
V
E
=10.2 Lmin
1
) and rapid pace (V
T
=498 208 ml,
f =28.4 16.4 bpm, and V
E
=14.1 Lmin
1
). A
2-min recovery period of normal quiet breath-
ing (V
T
=834 247 ml, 15.1 3.2 bpm, and
V
E
=12.6 Lmin
1
) was followed by a 20 s breath
hold, which concluded the measurements. Data
collection occurred under typical room conditions (air
temperature =24

C and 55% relative humidity).

Breathing frequency and V
T
was measured with
impedance plethysmography (Respitrak, Non-Invasive
Monitoring Systems, Miami Beach, FL). Before data
were collected, subjects were trained to maintain a
steady breathing pattern by watching the displayed
impedance plethysmograph output on a computer mon-
itor. Data were collected during 1 min of steady breath-
ing.
2.5. Data analysis
A principal aim in developing the oral temperature
probe is determining correlations between respiratory
air ows and oral cavity heat and mass transfer. Corre-
lations obtained from this study were calculated from
a minimum of 33 data points obtained from eight
268 J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277
subjects. Therefore, the minimum statistical power to
detect a correlation =0.6 with 95% condence was
0.967 (Sigma Stat for Windows, Jandel Scientic).
The rate of heat exchange between the airstream
and wall is described by the heat transfer coefcient,
h, which is dened by
q = hA
s
(T
s
T
a
) +
w
NM
w
A
s
(10)
where q is the heat transferred between the airstream
and surface, A
s
the surface area, T
s
the surface temper-
ature, T
a
the airstream temperature,
w
the latent heat
of vaporization, Nthe water ux across the surface, and
M
w
is the water molecular weight. The rst termon the
right hand side represents convective heat losses while
the second term accounts for evaporative heat losses.
Heat exchange in a non-wetted pipe is described by
only the rst term. For heat transfer within a conduit,
h can be dened in terms of a logarithmic temperature
difference, h
ln
,
q = h
ln
D
eq
L
_
_
(T
s1
T
a1
) (T
s2
T
a2
)
ln
_
T
s1
T
a1
T
s2
T
a2
_
_
_
(11)
where T
a
and T
s
are the airstream and surface temper-
atures, and subscripts 1 and 2 refer to inlet and outlet
conditions, D
eq
the equivalent diameter, and Lis the air-
way segment length =0.9 cm (distance between DBT2
and DBT4) (Bird et al., 1960).
The amount of heat transferred between the airway
wall and airstream is also reected in the change in T
a
as air passes through the airway segment:
q = mC
p
(T
a2
T
a1
) (12)
where m is the mass ow rate and C
p
is the specic
heat of air at constant pressure. Combining equations
(11) and (12), h
ln
can be dened as:
h
ln
=
mC
p
D
eq
L
_
_
(T
a2
T
a1
) ln
_
T
s1
T
a1
T
s2
T
a2
_
(T
s1
T
a1
) (T
s2
T
a2
)
_
_
(13)
Ananalogous equationfor the mass transfer coefcient,
k
ln
, during plug ow can be written as
k
ln
=
D
eq
v
4L
ln
_
C
si
C
ai
C
so
C
ao
_
(14)
where v is the mean velocity, water vapor concentra-
tions are given at the air/surface interface inlet, C
si
,
Fig. 6. Depiction of temperature probe placement in human oral
cavity. The probe was placed against the right buccal surface level
with the molars. The actual tongue position was somewhat different
during in vivo measurements, with the tongue attened against the
oor of the mouth.
and outlet, C
so
, and for the airstream inlet, C
ai
, and
airstream outlet, C
ao
(Skelland, 1974).
Equations (13) and (14) are solved using the tem-
perature data obtained with the multi-thermocouple
measurement system. Minimum inspiratory and max-
imum expiratory dry bulb temperatures averaged over
an entire trial were used to calculate h
ln
. Fig. 6 shows
the position of the probe within an idealized oral
cavity. During inspiration, T
a1
=DBT4, T
a2
=DBT2,
T
s1
=(DBT3 +DBT5)/2, and T
s2
=(DBT1 +DBT3)/2
while during expiration, T
a1
=DBT2, T
a2
=DBT4,
T
s1
=(DBT1 +DBT3)/2, and T
s2
=(DBT3 +DBT5)/2.
Similarly, k
ln
was determined from mean minimum
inspiratory and maximum expiratory humidities. The
appendix describes how C
ai
and C
ao
were determined
psychometrically from DBT2, DBT4, WBT2, and
WBT4. C
si
and C
so
were determined from T
s1
and
T
s2
using the Sonntag equation, an integrated form of
the ClausiusClapeyron equation (Laube and Holler,
1988).
The effect of on h
ln
and k
ln
was estimated by solv-
ing equations (14) and (15) after maximizing airstream
temperature differences by e
m
. Comparing h
ln
and k
ln
values for =50, 100, 250, 500, and 1000 ms showed
that raising from50 to 100 ms increased estimated h
ln
error by 34% while h
ln
error increased to 88% when
=1 s. Mass transfer rates were less sensitive to , k
ln
J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277 269
error increasing by only 26%when =100 ms and 43%
when =1 s.
Oral cavity D
eq
was calculated by modeling the
oral cavity as a rectangular channel with dimen-
sions obtained from Table 1. D
eq
for a non-circular
channel equals 4A/P, where A=(height)(width) and
P=2(height) +2(width) (Bird et al., 1960). Using
the anatomical dimensions listed in Table 1,
estimated channel height =(b
3
+b
5
)/2 and channel
width =(b
1
+b
4
)/2. During oral measurements, how-
ever, the mouth was only half open, so estimated chan-
nel height was reduced by half. Consequently,
D
eq
=
4
_
b
1
+b
4
2
__
b
3
+b
5
4
_
b
1
+b
4
+
_
b
3
+b
5
2
_ (15)
Pipe ow calculations were based on an internal diam-
eter =3.5 cm, half the hydraulic diameter calculated for
subjects oral cavities (Table 1). To compare human and
pipe heat transfer, experimental data were used to cor-
relate the Nusselt number, Nu, to the Reynolds number,
Re,
Nu =
1
Re
1
Pr
0.333
(16)
where and are constant coefcients, Nu =h
ln
D
eq
/k
t
,
k
t
the thermal conductivity, Re = vD
eq
/, the kine-
matic viscosity, Pr =/, =k
t
C
p
/, C
p
the specic
heat, and is the density. An analogous relationship
was used for mass transfer data, relating the Sherwood
number, Sh, to Re by
Sh =
2
Re
2
Sc
0.333
(17)
where Sh =k
ln
D
eq
/D
AB
, D
AB
is the diffusivity of water
in air, and Sc =/D
eq
.
Oral cavity morphology makes fully developed
parabolic ow unlikely to occur anywhere within the
oral cavity so modeling oral airow as plug ow in a
closed conduit also seemed appropriate. Experimental
and circular pipe ow results were compared to theo-
retical solutions for plug ow in a non-circular conduit
of mean oral cavity D
eq
(Table 1). Heat transfer coef-
cients take the form
N
1i
=
D
eq
ReN
2i
2L
_
1 4S
1 +4S
_
(18)
where
S =

2
n
exp
_
4
2
n
L
D
eq
N
2i
_
(19)
and N
1i
=Nu, N
2i
=Pr for heat transfer (Kay, 1963),
N
1i
=Sh, N
2i
=Sc for mass transfer (Skelland, 1974),
and
n
are roots to the equation J
0
() =0. The
rst six roots are
1
=2.405,
2
=5.520,
3
=8.654,

4
=11.792,
5
=14.931, and
6
=18.071.
One factor unaccounted for when comparing theo-
retical results to empirical oral heat transfer data is the
effect of mass transfer on heat transfer. Sensible heat
ux, q
s
, accounting for convective heat losses and heat
transfer by mass transfer, can be represented by
q
s
=
_

1 e

_
h
ln
(T
w
T
a
) (20)
where
=
NC
pw
h
ln
(21)
N=k
ln
(C
w
C
a
), C
w
and C
a
are the water vapor con-
centrations at the wall and airstream, respectively,
and

1e

=Ackermann factor, which accounts for

the effect of mass transfer on heat transfer (Skelland,
1974). Consequently, the percent change in the heat
transfer coefcient caused by mass transfer, HT (%), is
given by
HT(%) =
h
ln
h
ln
_

1e

_
h
ln
100 (22)
In addition, the effect of inaccurately measuring air
velocity due to inherent imprecision in impedence
plethysmography was tested by varying Re 30%.
3. Results
Representative oral cavity temperatures from a sin-
gle subject measured simultaneously with DBT15 and
WBT2 and WBT4 are shown in Fig. 7. Mean breath-
ing frequency =14.4 1.4 (S.E.M.) breaths min
1
and minute ventilation =31.0 4.2 Lmin
1
for all
subjects over the course of the study. Air velocity
averaged over the course of a breath was estimated
to range from 4.5 cms
1
(shallow, normal pace
breathing) to 11.4 cms
1
(deep, fast pace breathing).
270 J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277
Fig. 7. Dry and wet bulb temperature data simultaneously measured within the human oral cavity. These data are extracted from a 60 s trial with
the subject breathing at V
E
=19.6 Lmin
1
. Temperatures drop during inhalation and rise during exhalation as indicated. Note that airstream
temperatures have a much larger amplitude than buccal surface temperatures.
Mean lingual surface temperature (DBT1, DBT3, and
DBT5) =32.4 0.9, 32.0 0.9, and 31.9 1.1

C,
respectively. Lingual surface temperatures were
observed to drop steadily (approximately 1.2 0.3

C)
until subjects commenced rapid shallow breathing. It
was unclear whether this drop resulted from lingual
surface cooling resulting from the considerable
airow generated by deep breathing, slight distortions
of the lingual surface (causing reduced contact
between thermocouple and lingual surface) or a
combination of both factors. The ow rate (V
T
f)
did not signicantly impact the airstream temperature
gradient; DBT4 DBT2 =0.3 0.2

C with mean
peak differences =2.1 1.0

C. Likewise, the air-to-

lingual surface temperature gradient did not differ
signicantly as a function of ow rate. The proximal
air/surface temperature gradients during inhalation
(DBT4 surface temperature) =1.9 .7

C (largest
gradient =8.1 2.3

C) while the distal gradients

(DBT2 surface temperature) =2.0 .8

C (largest
gradient =7.9 2.3

C).
Among all subjects, the phase lag exhibited by
WBT sensors compared with DBT2 and DBT4 was
approximately 100 ms and caused by the larger mass
at the thermocouple tip. This phase lag caused wet
bulb temperatures to remain elevated well into much
of the inspiratory half-cycle despite dropping dry bulb
temperatures (Fig. 7). Surface temperature measure-
ments (DBT1, DBT3, and DBT5) also lagged behind
airstream temperatures (DBT2 and DBT4) because the
mucosal specic heat (1.0 cal g
1
C
1
) is roughly
four times greater than air (0.24 cal g
1
C
1
).
Figs. 8 and 9 compare heat and water vapor trans-
port measured in human oral cavities with physical
models (straight pipe, human airway castings) and
theoretical plug ow as a function of Re. Oral cavity
heat transfer data t equation (17) best when
1
=2.53
and
1
=0.70 for inspiratory data (r
2
=0.653, p <0.01)
and
1
=2.33 and
1
=0.698 for expiratory data
(r
2
=0.413, p <0.01). The two physical models used
to represent human in vivo oral cavity heat transfer, an
appropriately dimensioned straight pipe and Nuckols
et al. (1983) physical airway model, both underesti-
mate empirical heat transfer rates (Fig. 8). Empirical
pipe ow heat transfer data t equation (17) best when

1
=3.15 and
1
=0.514 (r
2
=0.71, p <0.01) but do
not correspond well to in vivo airway data. Nu values
obtained by Nuckols et al. (1983) in a plastic human
oral cavity casting were roughly an order-of-magnitude
less than pipe ow measurements and roughly two
order-of-magnitudes less than in vivo airway heat
exchange rates. In contrast, modeling oral inspiration
J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277 271
Fig. 8. Heat transfer in a circular pipe and human oral cavity as a function of ow rate. The non-dimensional heat transfer coefcient, Nu, was
calculated from temperature data obtained with the temperature probe. Reynolds numbers were computed from minute ventilation and based on
mean oral cavity dimensions. In vivo data outliers may be caused by dynamic changes in oral morphology or airstream temperature differences.
and expiration as plug owthrough a non-circular con-
duit t the empirical data well (inhalation: r
2
=0.64,
p <0.001; exhalation: r
2
=0.368, p <0.001; Fig. 8).
Oral cavity mass transfer coefcients are best t-
ted in equation (17) by
2
=0.00114 and
2
=1.53
during inhalation (r
2
=0.817, p <0.01) and
2
=0.175
and
2
=1.076 during exhalation (r
2
=0.710, p <0.01).
Theoretical plug ow in a non-circular conduit
(
2
=0.32719 and
2
=1.0 (inspiration),
2
=0.80
(expiration)) during both inspiration and expiration)
predictedinvivomass transfer rates closely(inhalation:
r
2
=0.496, p <0.001; exhalation: r
2
=0.503, p <0.001;
Fig. 9). Mass transport studies conducted with oral cav-
ity plastic castings either greatly overestimated (Cheng
et al., 1997) or underestimated (Hanna, 1983) empir-
ically measured in vivo water vapor transport. Fig. 9
shows that Cheng et al. (1997) observed mass transfer
rates during both inspiration and expiration orders-of-
magnitude greater than those observed in human oral
cavities. Results from Hanna (1983) greatly underes-
timated mass transport, especially during exhalation
(Fig. 9), and predicted inspiratory mass transfer rates
would exceed expiratory rates. In vivo empirical results
produced contrary results, i.e., expiratory oral cavity
mass transfer rates were greater than inspiratory rates
(Fig. 9).
Mass transfer had a negligible effect on sensible
heat transfer (approximately 1%), though evapora-
tive heat loss represents approximately 31% of the
total inspiratory heat losses at

V
E
= 16 Lmin
1
.
Total inspiratory heat losses partition into convec-
tive heat loss =0.859 cal s
1
and evaporative heat
loss =0.393 cal s
1
. Even with such large evaporative
losses, however, evaporative heat exchange does not
account for the large difference between human and
pipe heat transfer coefcients.
272 J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277
Fig. 9. Water vapor transport in the human oral cavity as a function of ow rate during inspiration and expiration. The non-dimensional mass
transfer coefcient, Sh, was calculated from psychometric data obtained with the temperature probe. The Reynolds number was computed from
minute ventilation and based on mean oral cavity dimensions.
4. Discussion
Oral cavity heat and water vapor exchange play
a major role in regulating overall respiratory tract
heat and water loss (Ferron et al., 1988b; Hanna,
1983; Ingenito et al., 1986; Kaufman, 1993) and,
consequently, inspired aerosol growth and deposition
(Larson, 1989; Martonen, 1993). Various models
(Cocks and McElroy, 1984; Larson, 1989; Martonen,
1993) have been proposed that explore the relationship
between inspired air properties (e.g., temperature,
gas composition, airborne particulates (both pharma-
ceuticals and pollutants), and pressure) and airway
health and injury during oral breathing. A lack of
empirical data on extrathoracic heat and water vapor
exchange rates have forced these models to depend on
theoretical predictions of oral heat and mass transport
based on numerical or physical models (Cheng et al.,
1997; Ingenito et al., 1986; Hanna, 1983; Nuckols
et al., 1983). The present effort is the rst work to
characterize human in vivo oral cavity transport and
offers an opportunity to improve the understanding
of physiological and physical processes during oral
breathing.
Study results demonstrate that oral cavity heat trans-
fer has been greatly underestimated in previous model-
ing studies (Nuckols et al., 1983). Similarly, modeling
has also failed to accurately predict in vivo oral cav-
ity mass transfer, both under- and overpredicting water
vapor exchange during respiration (Cheng et al., 1997;
Hanna, 1983). Why modeling has failed to more accu-
rately predict heat and water vapor exchange may be
attributed to the nature of previous models; anatomical
delity and physiological processes have been missing.
Accurately predicting oral heat and mass transfer
depends on how oral passage morphology is modeled,
with previous studies modeling the oral cavity as a
circular conduit (Daviskas et al., 1990). The present
J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277 273
results, however, show that Nu measured in a circu-
lar heated pipe differs so greatly from Nu measured in
the oral cavity that the validity of this assumption is
doubtful. This difference cannot be attributed to a lack
of water vapor exchange during pipe measurements
because in vivo mass transfer had a negligible effect
on sensible heat transfer.
Choosing to model the oral passage as a rectangular
conduit may also be somewhat arbitrary, though that is
the shape it appeared to assume during the present set
of experiments. It seems clear, however, that actual oral
cavity shape is irregular. Jaw and hard palate shape,
teeth position, and overall oral cavity dimensions
have considerable inter-subject variability. In addition,
buccal surface shape and tongue position and shape
change constantly and contribute to intra-subject
variability. Both inter- and intra-subject variability
contribute to observed data scatter. Improving heat and
mass transfer coefcient estimates requires synchro-
nizing oral passage shape estimates with temperature
measurements. Alternatively, comparing heat transfer
in variously shaped conduits with experimental human
data may be an appropriate methodology in establish-
ing an optimal model of oral cavity shape. Large-scale
physical models of the human oral cavity could then
be fabricated in which oral ow proles could be
established by using techniques developed by Hahn
(1992). Knowing oral ow proles could signicantly
enhance our understanding of air conditioning and
particle deposition during oral breathing.
Passing air through the oral cavity occurs under
widely varying conditions in terms of ow rate, sur-
face conditions (salivationandsurface wettedness), and
internal geometry. Lingual and buccal surfaces, along
with the soft palate, often change position. This alters
the internal geometry through which air passes, chang-
ing air velocity and residence time along oral surfaces
during both inspiration and exhalation. This in turn
affects evaporation and heat transfer rates from the
exposed tissues.
Models of the conducting airways appear to be reli-
able as they describe relatively rigid and geometrically
well-dened structures (trachea and bronchi). Physi-
cal oral cavity models (Nuckols et al., 1983; Cheng
et al., 1997), however, have not captured the dynamic
changes in geometry and lack potentially signicant
anatomical features (e.g., teeth, tongue, uvula, and ton-
sils) that contribute to oral surface area. Teeth increase
the wetted surface and airow turbulence, the uvula
likely acts as a n, enhancing heat and water vapor
exchange between oral surface and the airstream as a
function of h, while tongue and tonsils increase the oral
wetted surface area. Numerical models to date (Hanna,
1983; Ingenito et al., 1986; Ferron et al., 1988b) have
also been unable to capture highly complex dynamic
changes in oral cavity geometry. It is not a coincidence
that a detailed analytical model of oral cavity heat
and mass transfer remains to be developed; a greater
understanding of oral surfaces dynamics is necessary
before such features can be incorporated into a numer-
ical model.
Understandinghoworal anatomical structures affect
oral heat exchange mayalsoincrease our understanding
of respiratoryair conditioning. ComparingFigs. 7and8
for inspiratory ow shows an apparent lack of analo-
gous heat and mass transport commonly seen in uid
ow through conduits (Bird et al., 1960). Inspired air
owing over heat transfer ns (i.e., teeth) may serve
as a possible explanation. Dental surfaces, initially
moist but drying after a few oral breaths, act primarily
as a heat source for inspired air. Teeth will therefore
enhance inspiratory heat transfer without signicantly
altering mass transfer. Consequently, inspiratory air
will be signicantly warmed but not proportionately
humidied upon entering the oral cavity (and detected
by this studys instrumentation). In contrast, expired air
passing over oral mucosal surfaces will be both warmed
and humidied before reaching measurement devices.
Unsteady ow occurs during both inspiration and
exhalation as a function of intra-airway pressure gradi-
ents but corresponding changes in airow acceleration
are difcult to capture either analytically (Ingenito et
al., 1986) or empirically in physical models (Nuckols
et al., 1983; Hanna, 1983; Cheng et al., 1997). Higher
velocities during the initial stages of inspiration and
expiration are accompanied by higher heat and mass
transfer rates. Air velocity (along with heat and mass
exchange) decreases as the pressure gradient between
the lower and upper airways diminishes until it reaches
zero and ow reverses. Modeling deviations from in
vivo air velocity proles can only exacerbate prob-
lems in model delity. Advances in computational uid
dynamics may allowthis issue to be addressed in future
modeling efforts.
Oral respiration occurs where minute ventila-
tion exceeds roughly 30 Lmin
1
(Niinimaa et al.,
274 J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277
1981), common during physical exertion or disease
(e.g., emphysema). Nasal obstruction or volitional
inspiration of pulmonary medications can also elicit
oral breathing, even at minute ventilations below
30 Lmin
1
. Aerosols entering the oral passage expe-
rience a geometrically simpler path to the conducting
airways compared to nasal breathing (due to nasal
turbinates), thus inertial impaction and interception
play lesser roles in eliminating aerosol droplets and
particulates from the respiratory airstream. For this
reason, the oral cavity is commonly used to introduce
pharmaceuticals into the lower airways as an aerosol
(e.g., asthma inhaler). Unfortunately, oral breathing
may also expose lower airways to greater risk of injury
from inspired pathogens or toxins.
Aerosol deposition proles along the tracheo-
bronchial tree and pulmonary airways are size
dependent as a function of both initial (inhaled)
dimensions and subsequent growth during passage
along the airway (Ferron et al., 1988a; Martonen,
1993). Larger aerosols (>10 m) exiting the oral
cavity generally have sufcient inertia to impact the
oropharyngeal wall while smaller particles follow
airow streamlines, pass into the larynx, and deposit
along the conducting airways as a function of MMAD
(Ferron et al., 1988a; Martonen, 1993).
Hygroscopic particles can grow within the oral
cavity, e.g., relatively small particles (<10 mm) may
adsorb sufcient water vapor (and inertia) to impact
the oropharynx and thus fail to travel into the lower air-
ways. This growth depends on particulate (or droplet)
hygroscopicity and is largely determined by the ef-
ciency of heat and mass transfer between aerosol and
oral surfaces. As this work has demonstrated, oral heat
and water vapor exchange are signicantly affected
by ow characteristics and geometry, suggesting that
these factors strongly inuence aerosol growth in the
oral cavity.
Aerosol deposition proles strongly affect the ef-
cacy of therapeutic interventions (e.g., asthma inhalers)
along with vulnerability to disease and injury (e.g.,
chronic inhalation of airborne acid droplets; Cocks and
McElroy, 1984; Larson, 1989). Therapeutic inhalers
are designed to produce aerosol droplets or particulates
optimized for depositing onto bronchial surfaces; these
product designs are based on existing models of lower
airway particle deposition. Underestimating oral cav-
ity aerosol growth results in overestimating the mass
and number of droplets or particulates delivered to the
site of action. This probably results in unrealized ther-
apeutic efcacy and a reliance on unnecessarily large
discharged mass from inhalers. A greater understand-
ing of oral cavity heat and mass transport can improve
pharmaceutical delivery (i.e., deposition in extratho-
racic airways) and efciency by redesigning inhalers
to account for realistic oral aerosol growth.
Likewise, our current understanding of adverse
consequences associated with inhaling pathogenic or
toxic aerosols may be inadequate since oral cavity
particle growth appears to be generally underestimated
in existing models of aerosol deposition. Greater oral
aerosol growth will reduce conducting and pulmonary
airway exposure to pathogens and toxins but increase
extrathoracic airway exposures. This suggests that
increased airstream velocity, buccal surface drying,
altered oral geometry, or smaller initial aerosols might
be necessary to account for lower airway infections.
This may also partly explain why ambient tem-
peratures correlate with respiratory illness in colder
weather. Nasal congestion is often experienced in cold
weather because of increased nasal water vapor con-
densation as exhaled air passes over the relatively cool
nasal surfaces. This condensation partially blocks the
nasal passages, both directly and possibly indirectly
by promoting mucosal swelling due to osmotic pres-
sure changes, which elevates nasal pressure drop and
promotes oral breathing. Inhaling colder, drier air may
reduce oral humidity and decrease hygroscopic aerosol
(e.g., bacterial or viral laden droplets) growth, allow-
ing a larger aerosol mass to pass into the conducting
and pulmonary airways. Respiratory defense mecha-
nisms will ultimately be overwhelmed given a suf-
cient deposited pathogen mass. Reduced dental sur-
faces in fully or partially edentate individuals (e.g.,
young children, elderly individuals) may also con-
tribute to airway disease because reduced oral heat and
mass transfer due to missing heat transfer ns (i.e.,
teeth) will likely increase lower airways deposition of
inhaled pathogenic aerosols.
This paper describes how a temperature probe used
to simultaneously measure airstream and buccal tem-
peratures at multiple sites was developed and tested.
Acquiring temperature data simultaneously avoids
errors in computing h
ln
and k
ln
associated with tempo-
ral and spatial changes in oral cavity morphology and
surface blood ow patterns. This is an improvement
J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277 275
over sequential temperature measurements previously
used for determining h
ln
(Eisner and Martonen, 1989;
Ingenito et al., 1987; Primiano et al., 1984). Sequen-
tially measurements introduce errors because any oral
cavity shape changes occurring between measure-
ments will cause airow patterns to change and alter
airstream temperature distribution. Transient changes
in ambient conditions between measurements may
also modify buccal blood ow (Fouke et al., 1990). In
addition, sequentially placing a probe in well-dened
locations vis-a-vis previous measurements is difcult
and contributes to measurement errors.
Establishing probe accuracy was accomplished
in two ways. First, we estimated probe accuracy
fromthermocouple response times. Estimated dynamic
errors <5%and steady state errors of 3 and 11%for dry
and wet bulb temperatures, respectively, suggest that
data obtained with the probe was accurate. Comparing
h
ln
measured in a heated pipe with a theoretical solution
for plug ow validated the error estimates. The close
correlation shown in Fig. 8 between tted pipe data
and theoretical plug ow values veries that the probe
accurately measures dynamic temperature changes.
Humidity measurement accuracy can be improved
by reducing WBT response times. Thermocouple tip
size cannot be appreciably reduced without sacric-
ing durability. However, Eisner and Martonen (1989)
demonstrated that reducing wet bulb mass considerably
reduces response times. Using a mass spectrometer to
measure humidities avoids this problem but increases
sampling complexity and adds the question of transit
times. Our design had the advantages of durability and
simplicity and could be easily repaired. Future probes
using our design can reduce steady state errors by mini-
mizing the cotton mass at the thermocouple tip without
abandoning our design.
In summary, this study quantied in vivo oral cavity
heat and mass transfer and identied factors that might
contribute to improved pharmaceutical delivery and
also explain a propensity among some individuals to
airway disease. Results suggest that additional efforts
to characterize upper airway processes are needed
before we can truly understand airway health and
injury. This study also demonstrates the limited value
of physical and numerical models in describing heat
and water vapor exchange in a geometrically complex
and dynamic respiratory region. Critical to this effort
was development of a unique temperature probe that
determined oral cavity humidity and temperature
during normal breathing and permitted experimental
measurements of human oral cavity water vapor
exchange for the rst time. This probe can also be
used in future work to identify oral factors, such as
impaired oral cavity water exchange, contributing to
susceptibility to airway disease and injury.
Acknowledgements
Human subjects participated in this study after giv-
ing their voluntary informed consent. The authors wish
to thank Dr. Peter Scherer for his suggestions in writing
this paper. The views expressed herein are solely those
of the authors and should not be construed as the of-
cial policy or position of the Department of Defense or
Department of the Navy.
Appendix A. Computational basis for
determining airstream humidity
Airstream water vapor concentration can be dened
in terms of the water vapor mole fraction in the
airstream, X
w
, by:
C
a
=
X
w

a
(1 X
w
)28.965
(A.1)
where
a
is the density of dry air and
28.965 =molecular weight of dry air. Dry air
properties were used for simplicity in calculations.
Using saturated air properties for 37

C air increases
calculated density and C
a
by only 2%. The water
vapor mole fraction in a saturated air sample at the
airstream temperature and pressure, X
ws
, is related to
the saturated water vapor partial pressure, P
ws
:
X
ws
=
P
ws
P
(A.2)
where P is the total pressure of moist air. Airstream
relative humidity, , is the ratio of the airstream water
vapor mole fraction, X
w
, to X
ws
:
=
X
w
X
ws
(A.3)
276 J.W. Kaufman, K. Farahmand / Respiratory Physiology & Neurobiology 150 (2006) 261277
Combining equations (A.2) and (A.3),
X
w
=
P
ws
P
(A.4)
P
ws
is related to airstream wet bulb temperatures, T
wb
,
by:
P
ws
= exp
_
C
1
T
wb
+C
2
+C
3
T
wb
+C
4
T
2
wb
+C
5
T
3
wb
+C
6
ln(T
wb
)
_
(A.5)
where the C
i
(i =1, . . ., 6) are constants (ASHRAE
Handbook, 1985). The humidity ratio of saturated
moist air, W
s
, can be determined from equation (A.5)
by
W
s
= 0.62198
P
ws
P P
ws
(A.6)
and the airstream humidity ratio, W, can be calculated
from
W =
(1093 0.556T
wb
)W
s
0.24(T
db
T
wb
)
1093 +0.444(T
db
T
wb
)
(A.7)
where T
db
is the airstream dry bulb tempera-
ture (ASHRAE Handbook, 1985). It should be
noted that actual saturation humidities are at least
0.30.5% higher than calculated from equation (A.6)
because water vapor deviates from ideal gas behavior
(Zimmerman and Lavine, 1964). At the temperatures
of interest, however, this error is probably 1.0% and
so has been neglected. The degree of airstream satu-
ration, , can be determined by combining equations
(A.6) and (A.7):
=
W
W
s
(A.8)
and allows to be calculated from:
=

(1 )
_
P
ws
P
_ (A.9)
Airstream water vapor concentrations can then be
determined fromexperimentally measured T
wb
and T
db
by combining equations (A.1), (A.4), (A.5), (A.8), and
(A.9).
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