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Tooth Pulp Tissue Pressure and Hydraulic Permeability: by Arthur C. Brown, PH.D., and David Yankowitz, D.D.S., M.S.D
Tooth Pulp Tissue Pressure and Hydraulic Permeability: by Arthur C. Brown, PH.D., and David Yankowitz, D.D.S., M.S.D
Hydraulic Permeability
By Arthur C. Brown, Ph.D., and David Yankowitz, D.D.S., M.S.D.
• If the pulp chamber of a tooth is pene- The object of this paper is to characterize
trated, either by dental caries, or by a dental the forces involved in a fluid exchange within
drill, inflammation and eventual death of the the tooth pulp chamber of the dog. Specifical-
pulp tissue usually follows. While a long in- ly, we have attempted to measure the tissue
terval may elapse before degeneration is com- pressure of the tooth pulp (if pressure is the
plete, necrosis is an almost inevitable conse- correct term) under static conditions, i.e.,
quence of pulpal penetration. when no net exchange of fluid is taking place,
A current explanation in the dental litera- and to measure the dynamic resistance to fluid
ture for this phenomenon is as follows.1 The exchange (in other words, the hydraulic
application of noxious stimuli to the dental permeability) of the tooth pulp tissue.
pulp is followed by inflammation of pulp tis-
sue and release of fluid into the dental pulp Methods
canal. This is supported by histologic evi- Adult mongrel dogs weighing 10.5 to 15 kg
dence of edema, polymorphonuclear leukocy- were used. Measurements were made on the
tic infiltration, and disorganization of the odon- maxillary third incisors and the maxillary and
toblastic layer in pulp of teeth which have mandibular canines. Each tooth was used in only
one experiment; however, each animal was em-
been diagnosed as suffering from acute pulpi- ployed in several experiments until all suitable
tis.2 The inability of the dental pulp to recover teeth had been used.
easily from noxious stimulation is claimed to The animals were anesthetized with pentobar-
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be due to the rigidity of the dentin walls sur- bital sodium (Diabutal, Diamond Laboratories),
rounding the pulp. This rigidity prevents injected intravenously. Also, the tranquilizer pro-
swelling characteristic of soft tissue inflamma- piomazine hydrochloride (Largon, Wyeth) was
injected intramuscularly to reduce the amount of
tion and thus leads to an increase in pulp pentobarbital necessary to maintain the anesthetic
tissue pressure.3 The pressure eventually be- level. A thermistor probe was inserted rectally
comes high enough to impede circulation, for continuous observation of deep body tempera-
causing pulpal ischemia and subsequent tis- ture. By means of external heating or cooling, the
sue death. The vascular supply of the dental rectal temperature was maintained at 38°C ±
pulp enters and leaves through tiny foramina 0.5°C. Room temperature was maintained at
20°C to avoid spurious pressure readings due to
at the apex of the root and thus is particularly expansion or contraction of the fluid in the measur-
susceptible to the increased tissue pressure. ing system.
While this hypothesis seems reasonable, it can The enamel was penetrated with a #X round
neither be completely accepted nor rejected dental bur driven by a low speed dental motor.
due to the lack of information about the Subsequent drilling was done manually with
mechanical and hydrostatic forces within the small twist-drills mounted in a watchmaker's pin
vise.
pulp chamber. The original hole (produced by the bur) was
extended 2.50 mm toward the pulp with a #79
drill (diameter 0.37 mm). This hole was enlarged
From the Department of Physiology and Biophysics with a #72 drill (diameter 0.63 mm) but only
and the Department of Endodontics, University of to a depth of 2.25 mm and further enlarged with
Washington, Seattle, Washington. a #71 drill (diameter 0.655 mm) to a depth of
Supported in part by Grant DE 7103 from the 2.00 mm, forming a tapered hole to produce a
National Institute of Dental Research. tight "jam" fit when the threaded needle was
A preliminary report of this work has appeared in later screwed in.
abstract form. Physiologist 6: 301, 1963. The #79 drill was then reused, this time with
Received for publication December 16, 1963. a series of sleeves slipped over it to allow pene-
42 Citcaltiion Research. Vol. XV, July 1964
TOOTH PULP PRESSURE 43
tration in 50-micron increments. These sleeves potentiometric recorder. The maximum error in
were constructed from 22-gauge stainless steel pressure measurement was ± 2 mm Hg, and was
hypodermic tubing, and ranged from 0.750 mm to due both to drift in the apparatus and to reading
2.000 mm in length with intervals of 0.050 ± 0.005 error.
mm. Since the mechanical force retarding the Before connecting the cannula to the tooth,
advance of the drill is greatly reduced as the the compliance, leakage rate, and response time
pulp chamber was entered, the sleeves were of the system were checked. The compliance of
necessary to prevent deep penetration of the measuring system was determined by screwing the
pulp and resulting tissue damage. By using cannula into a blind hole, thus producing a
progressively shorter sleeves, the hole was ex- closed system. The microsyringe was advanced
tended toward the pulp chamber until either (or withdrawn) in several steps, recording simul-
clear fluid or fluid mixed with blood was seen taneously the volume injected and the pressure
rising in the hole. obtained. The compliance (C) of the system was
At this point a threaded stainless steel cannula calculated from the ratio of the volume (V) incre-
was screwed into the hole. The cannula was made ment divided by the pressure (P) change, or
from 22-gauge stainless steel hypodermic needle
tubing (outer diameter 0.75 mm, inner diameter dV
C- (i)
0.40 mm) threaded at one end with a jeweler's
die. The other end of the cannula was tapered The compliance was constant over the total range
and connected to a 30-cm length of PE 50 poly- of pressures examined, and had a value of
ethylene tubing which led to a pressure trans- 1.5 X 10~-s ul/mm Hg. Leakage was checked by
ducer (Sanborn model 267B). A microsyringe elevating the pressure in the closed system to
(Gilmont microburet) with a capacity of 100 a\ between 90 and 100 mm Hg and allowing it to
and a resolution of 0.01 fil was connected to trie remain at this level for some time; the rate of
other inlet of the pressure transducer (fig. 1). pressure drop indicated the magnitude of the
The entire hydraulic measuring system (syringe, leak. By careful attention to all connections, it was
pressure transducer, cannula, and connecting tub- possible to reduce leakage rate to 0.2 ^,1/hr or
ing) was originally filled with water, taking care less. The cannula-tooth junction was tested for
to eliminate all air. On the day of the experiment, leak rate by screwing the cannula into the tooth
about 80 ftl of the water were expelled and at the beginning of an actual experiment but
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the needle refilled with an equal amount of with the hole extended only partly through the
mammalian Ringer's solution to avoid introducing dentine and not into the pulp; no leaks were
a nonphysiological solution into the tooth pulp found at this junction.
cavity. During the period of screwing the threaded The response time of the measuring system was
needle into the tooth, the microsyringe was manip- less than 0.2 second; the actual value was too
ulated to eject fluid continuously and prevent rapid to be accurately registered by the Varian
trapping of air in the hole. recorder. (The recorder response was too slow
The pressure transducer output was amplified to indicate pulse waves. .However, simultaneous
by a Tektronix type Q carrier preamplifier; a observation on an oscilloscope showed a variable
Tektronix type 133 power supply provided power pulse pressure of several mm Hg.)
for the preamplifier and an additional stage of
gain. This signal was recorded by a Varian Upon completion of each experiment, the
cannula was unscrewed and held at tooth level
to obtain the zero base line for pressure measure-
ments. Since the animal was in a supine position,
the mouth was approximately at heart level.
Hence the pressure measurements may be con-
PE tubing sidered as referred to heart level as well as tooth
carrier 0 JO 100
level. The hole was then sealed with a temporary
a/np
Tooth filling made from eugenol and zinc oxide. Upon
Detail
recovery, the animal showed no particular dis-
pulp comfort or disability, either of a general nature or
^cannula
f . tnhlng pen recorder of mastication.
countersink
370-u hole Results
PULP PRESSURE
FIGURE 1
Schematic illustration of the measuring apparatus. After insertion of the threaded cannula into
Detail at lower left indicates the method of tapping the tooth a few minutes were allowed to
the pulp chamber. elapse. During this interval the pressure in
Circulation Rtsmrcb, Vol. XV, July 1964
44 BROWN, YANKOWITZ
cc
system; thus this reading was taken as a
measure of the equilibrium pulp pressure 30
(PeQ). However, this method is open to the a:
criticism that the pressure recorded may not 0. 27 28 29 30 31
be characteristic of the pulp in the natural
state, since the procedure of screwing in the
cannula or of injecting fluid may have trapped
100
and compressed liquid which could not es-
cape. If such was the case, this measurement 3 , 9°
would be more an index of the elastic com-
pression modulus of the pulp tissue than of the E
pulp tissue pressure. E 70
In order to test this possibility (as well as U 60
to calculate the hydraulic permeability), fluid cr
3 50
was either injected into or withdrawn from the in
system using the microsyringe. As shown by U4O
the typical record of figure 3, the pulp pres- °-30
sure ultimately returned to similar values fol- 21-3-63
lowing either injection or withdrawal. This 37 38 39 40 41 42
was true whether a single injection was made TIME (min)
or whether a series of successive injections
FIGURE 3
preceded final equilibration. The final level
Sample record of pressure changes following injection
was also independent of the size of the in- (lower trace) or withdrawal (upper trace) of about
jection. The equilibration level was close to 0.08 id of fluid.
Circulation Rtsetrcb, Vol. XV, Inly 1964
TOOTH PULP PRESSURE 45
TABLE 1 finally reaching a steady value. Since the meas-
Hydrostatic Pressure and Hydraulic Permeability of uring system behaved as an elastic container,
Tooth Pulp and since the volume of fluid in the micro-
Permeability * syringe did not change after the initial injec-
DOE Tooth Pulp pressure f<P.q tion, the drop in pressure could have been due
mm Hg fil, hr-mm Hg
1 Lower right canine 58-70 only to the loss of fluid from the measuring
Lower left canine 62-76 0.59 0.27 system. This fluid must have flowed into the
Upper right lateral 48-51 0.17 0.17 tooth. Similarly, the pressure rose following
Upper left lateral 57-78 0.20 0.08 an initial drop caused by withdrawal of fluid
2 Lower right canine 67-77 0.25 0.06 into the syringe (fig. 3, top); this rising pres-
Upper right lateral 45-50 0.50 0.12 sure could have been due only to fluid passing
Upper left lateral 41-55 0.45 0.20
3 Lower right canine 52-61 from the pulp chamber into the measuring sys-
Upper left canine 38-47 0.12 0.08 tem. The rate at which the pressure returned
Mean 57 0.33 0.14 to its steady level was an index of the rate of
exchange of fluid with the dental pulp.
* Values for which P > Peq indicate flow into the
tooth; for P < Peq, flow is out of the tooth. The per- A quantitative relation between flow and
meability measurements are the average dQ/dP in the pressure change can be derived from the fol-
range from 0 to 20 mm Hg above or below Peq. lowing considerations. The flow rate (Q) is
equal to the rate of change of volume (V)
pulp penetration. This range includes both with time (t) in this system, or
random pressure variations, hysteresis effects,
and tendency of the mean pressure to drift (2)
with time. The average value of pressure for
all teeth was 57 mm Hg. However, when the volume of the micro-
The pressure was not always constant in syringe is not changing, alterations in volume
in the measuring system are reflected in pres-
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eral is greater when P>Peq than when this and other teeth tested are listed in table 1.
P < P^. For this curve, average values for the The flow-pressure curve for a given tooth
was reproducible if the measurements were
CuL/hr) CnL/mln) taken within a period of a few hours. How-
- 150 ever, if the permeability measurements were
8 extended over a long time (4 to 6 hours),
* the final flows at a given pressure were often
6 * -100
• appreciably below those initially obtained.
4 This was particularly true for the permeability
Into * _- 5 0
2\ tooth \ : values for fluid flow into the dental pulp.
i yff* i • • Discussion
So •
ACCURACY OF THE EXPERIMENTAL MEASUREMENTS
• • •
2
out of -50 Besides the usual errors associated with
4 • tooth ; pressure measurements, this experiment had
two particular sources of error which could
6 : * -
have led to large inaccuracies. The first con-
20 40 60 80 100
PRESSURE (mm Hg)
cerns the great sensitivity of the system to
small leaks. For example, it may be seen from
FIGURE 4 figures 4 and 5 that a leak rate of 2 /tl/hr
Flow calculated from equation 3 as a function of aver- (about one average-sized drop per day) would
age system pressure. Each point represents a separate have led to an apparent equilibrium pres-
measurement. Left, microliters (1CH liters) per hour;
right, nanoliters (10-' liters) per minute. Records sure some 40 mm Hg below the true value.
shown in figures 2 and 3 and data on this graph come This sensitivity is not due to any deficiency
from the same tooth (dog 2, lower right canine). of experimental design, but rather is caused
Circnlttion Raesrcb, Vol. XV, July 1964
TOOTH PULP PRESSURE 47
by the inability of the tooth to furnish even the fluid seen rising in the hole was seen to
small amounts of fluid without a large pres- be tinged with blood; in other experiments
sure drop. The magnitude of the error caused clear fluid was seen rising in the hole, indicat-
by leaks may be estimated by multiplying the ing that tissue damage was minimal or ab-
leak rate times the hydraulic permeability of sent. Yet, the results in the former experiments
the tooth at P«j. By careful attention to all were not significantly different from those in
connections, it was possible to get the leak the latter experiments. (2) Since blood flow-
rate below 0.2 /tl/hr, leading to a maximum er- ing in the tooth pulp capillaries presumably
ror of —4 mm Hg. Since the pressures through- has not lost the ability to clot, this hypothesis
out the experiment are always positive (great- would predict that the initial measurements
er than atmospheric), the effect of this error should be high, later measurements declining
is always to cause the apparent Peg to be toward true tissue pressure as the severed
lower than the true value. vessels closed. In fact, the opposite was seen,
Another possible source of inaccuracy de- the major systematic trend with time being a
pends upon the system compliance. As can be steady rise in P^. (3) Blood clots were not
seen from equation 3, the greater the com- usually formed in the needle or tubing even
pliance, the slower the rate of change of pres- during those maneuvers in which tissue fluid
sure for a given flow rate. Thus, a high com- was withdrawn from the pulp. (4) It is diffi-
pliance will lead to a very slowly equilibrating cult to imagine a mechanism whereby a sev-
system. The compliance of the system em- ered vessel can pour out less fluid when un-
ployed in this experiment was very small, usu- obstructed than it can accept when the sur-
ally allowing equilibration in a few minutes rounding pressure is raised. Yet, the tooth
even with the small flow rates characteristic pulp was able to accept fluid much more
of the dental pulp and permitting measure- readily than it was able to exude fluid.
ment of flows to a resolution of 0.1 /il/hr. The most probable explanation of these
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fore any fluid had been injected from the hypothesis of passive exchange of water
system into the tooth. through the dental capillary wall.
In summary, the most likely hypothesis is A high capillary pressure implies, however,
that the equilibrium pressure represents the that hemodynamics of the dental pulp circula-
normal hydrostatic pressure found in the tooth tion must be considerably different from most
pulp canal. other body tissues. In contrast to "typical"
tissue in which the major drop of blood pres-
DENTAL PULP TISSUE PRESSURE
sure occurs in the arterioles and precapillary
The experimental measurement of Peq and sphincters,"'I0 in the dental pulp circulation
its identification with pulp tissue pressure a major part of the pressure drop must occur
leads to the following description of dental in the venules and veins.
pulp forces. The anatomy of the pulp provides a basis
(a) Free interstitial fluid appears to exist for the development of high capillary pres-
within the dental pulp and, thus, the forces sures. The small size of the apical foramina
within the pulp can be described accurately in through which the vessels must pass means
part as hydrostatic pressures. The only finding that a relatively high hemodynamic resistance
not consistent with this conclusion is the may be developed at this point. In addition,
variable degree of "hysteresis." This may imply since the collecting vessels are contained in
that hydrostatic forces are not rapidly trans- the same rigid chamber with the rest of the
mitted to all parts of the pulp, allowing local pulp, the high hydrostatic tissue pressure will
tissue distortion to produce local pressure al- be transmitted to the venules and veins, tend-
terations, (b) This pressure is relatively stable ing to make them collapse and raising their
and is much higher than that found in most resistance to flow.
other tissues.4'n It is noteworthy that high This view suggests that in dental pulp the
interstitial pressures have also been recorded circulation of blood may be in a rather pre-
for renal tissue and that both the kidney and
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within the pulp vascular system. Thus, each stitial space requires a greater pressure gra-
injection from the measuring system into the dient than the efflux of fluid in the opposite
pulp may compress the tooth vessels, squeez- direction. The tissue distortion that may result
ing blood from the pulp canal. However, as from injection or withdrawal forms another
the volume which can leave the tooth in such possible explanation for the shape of this
a manner is limited, this explanation is highly curve. Perhaps the increased pressure at the
improbable since Pcq does not increase sig- site of injection causes tissue to be pushed
nificantly following a series of injections, re- away from the hole and even causes fissures to
gardless of the number and size of the in- develop disrupting the gelatinous matrix of
jections. the pulp, thereby exposing a relatively large
The alternative and more probable explana- capillary surface area to fluid exchange. On
tion is that fluid which leaves the tooth upon the other hand, lowering the pressure at the
injection is interstitial tissue fluid. Most of hole tends to make the pulp collapse against
this fluid probably passes into the pulp capil- it, thereby decreasing the available surface
laries and is thus removed from the tooth. area. According to this explanation, the non-
However, some fluid may pass out through the linearity is a reflection of the differing surface
apical foramina in the space external to the areas available for the two processes. Implicit
apical blood vessels. in this latter view is the assumption that pres-
Thus, the process assumed to generate the sure alterations are not immediately dis-
curves of figure 3 is as follows. The first effect tributed equally throughout the pulp. Which
of rapid ejection of fluid from the micro- of these explanations is correct cannot be
syringe is an increase in the volume of fluid answered from the data at hand but rather
in the remainder of the measuring system requires further investigation of the detailed
without a significant amount of fluid passing pattern of fluid distribution.
into the tooth. This leads to an increase in
Summary
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