lntraureteric pressure above and below an area of compression GURAN
ENHORNING,
ROBERT Salt
Lake
G. City,
WEAVER,
M.D.* M.D.
Utah
I T H A s been known for more than 100 years that the renal pelvis and ureter dilate during pregnancy. 1 Endocrine changes resulting in a relaxation of the smooth musculature of the ureter are considered an important etiologic factor.2-6 However, since the right ureter is more apt to become dilated than the left, and since there is hardly any dilatation below the pelvic brim, it is generally accepted that hormonal changes alone do not fully explain the ureteral dilation typical of late pregnancy. There must also be a mechanical compression between the presenting part of the fetus and the pelvic brim.3, i, * This will lead to a urinary stasis which, because of dextrorotation of the uterus and the protection the sigmoid offers to the left ureter, is more apt to be pronounced on the right side. Ureteral compression also is frequently encountered in gynecology. If the cause is a pelvic tumor, this may be surgically removed, but in the case of a malignancy removal is not always possible. The fact that ureteral obstruction, leading to renal failure, is the leading cause of death among
patients with carcinoma of the cervix9 accentuates the need for increased knowledge of a ureter’s ability to cope with compression. Intraureteric pressure recordings in humans have shownlo’ l1 that during diastole, i.e., the rest period between peristaltic contractions, there is a complete relaxation of the ureter, but that during systole pressure may increase from 18 to 100 cm. of water. If the pressure in the ureter in an area of compression is consistently near this value, transportation of urine to the bladder would be jeopardized. The purpose of the present experimental study in dogs was to ascertain whether or not the ureter, when compressed to pressures near the normal systolic value, is able to react with increased systolic pressure or with other means of overcoming an increased resistance. The lower ureter was subjected to a compression of 50 or 100 cm. of water over a 1 cm. length, above and below which intraureteric pressure was simultaneously recorded. MdlOdS
Pressure recording. For simultaneous transmittance of pressure from two points in the ureter a double lumen catheter was used. Its principle has been described in detail elsewhere.12 The catheter used in this study was 40 cm. long and was made of polyethylene tubing PE 10 (inner diameter 0.28 mm., outer diameter 0.61 mm.) introduced into PE 60 (inner diameter 0.76 mm.,
From the Departments of Obstetrics and Gynecology and Surgery, University of Utah, College of Medicine. This work was supported in part from National Institutes of Health funds, Grant No. FR-05128. *Present address: The Karolinska Institute, Department of Obstetrics and Gynecology, Sabbatsberg Hospital, Stockholm, Sweden.
1332
lntraureteric
pressure
and
compression
1333
Fig. 1. Tip of catheter used for transmittance of intraureteric pressure. Through separate canals flaccid balloons communicate with each a transducer.
outer diameter 1.22 mm. which is the French scale 3.6). The two channels thus obtained communicated with thin-walled rubber balloons, which had been threaded over the catheter and which were 5 cm. apart (Fig. 1) . The balloons as well as the channels of the catheter and the chambers of the transducers contained liquid, and particular care was taken to avoid air bubbles. The balloons were flaccid and there was no tension in their walls. From each of the balloons pressure was transmitted to transducers (Sanborn Model 267 A). A direct writing two-channel recorder was used. For calibration the catheter was introduced into a glass tube in which it was subjected to known ‘hydrostatic pressures. This was done just prior to and immediately after each examination. Compression of ureter. It was desired to subject the ureter to a known amount of compression while intraureteric pressure was being recorded. For that purpose a compression device was used. Its principle was that of a sphygmomanometer cuff. It consisted of a piece of lucite 0.2 by 1 by 8 cm., bent like a hair pin and outlined with a thin-walled tubing. The device was applied around the ureter which could then be compressed by raising a water bottle which communicated with the tubing (Fig. 2). The bottle was raised so that its liquid surface was 50 or 100 cm. above the level of the ureter. When no compression was desired the bottle was held below this level. Material and procedure. The technique was applied first in a pilot study of 4 dogs, following which a series of 8 male and 2 female dogs were examined. They consti-
Fig. 2. Technique of compressing ureter and simultaneously recording intraureteric pressure above, A, and below, B, the area of compression.
tuted a heterogenous group in regard to breed and size (Table I). Dog No. 7 was so small the catheter met resistance when introduced, and due to technical difficulties the ureter was not subjected to compression. The dogs were anesthetized with pentobarbital sodium (25 mg. per kilogram) I The bladder and lower ureter were exposed through a midline incision. An approximately 2 cm. long portion of the lower half of the ureter was dissected free in order to allow the compression device to be applied. The latter was introduced into the abdominal cavity through a stab wound in the flank. A longitudinal incision in the ureter, close to its junction with the bladder, allowed the pressure measurement catheter to be introduced. It was gently pushed up in the
1334
Enhiirning
and Weaver
Table I. Ureteral
activity
prior
to compression
Pressure Upper Dog No.
Weight (Kg.)
1 2 3 4
25.4 26.3 20.4 20.9
65 7 8 9 IO
30.9 13.6 10.0 20.0 18.9 20.4
Between per~st~~tic Sex
f ii : d ij
waves 0 0 25 5 15 10 5 0 0 5
in ureter
tracing
in cm.
of water Lower
Peak of contraction
85 115 120 90 115 65 80 85 60 125
tracing
Between per~stalt~c waves
5 0 35 0 0 10 5 5 0 0
Peak o# contraction
70 105 125 50 110 75 95 95 85 180
Frequency contractions per min.
9 7 17 8 7 10 20 9 6 3
Speed of peristaltic waues cm. per second
4
Fig. 3. Upper tracing from balloon A, above compression device. Lower tracing from balloon B (Fig. 2). Note that in lower tracing the introductory nodular pressure increase marked with arrow disappears as soon as compression is applied.
until the balloon at the tip (marked A in Fig. 2) had just passed the compression device. That the pressure measurement catheter was in the right position, i.e., with one balloon above and one below the portion of the ureter which was to be compressed, was checked by light palpation. Just after the catheter had been introduced the ureter was frequently in a state of hyperactivity but within a few minutes this subsided and its peristalsis became regular. Without compression, the activity of the ureter
ureter was followed for at Ieast 30 minutes. It was then subjected to a period of compression after which it was left untouched. It then usually re-established the peristalsis it had prior to the compression. In one dog (No. Z), in which the results of four compressions were very conspicuous, a fifth experiment was performed under slightIy dtered conditions. To prevent a build-up of pressure above the area of compression the upper ureter was drained with a catheter which was introduced through a longitudi-
pressure and compression ‘1335
intraureteric
nal incision immediately above the upper balloon. Since the response was almost instantaneous, and since it usually disappeared very soon after release of the compression, a single ureter could be subjected to repeated experiments and each dog could serve as its own control. Results
Recording prior to compression. As may be seen from Table I the intraureteral pressure between contractions was low. It ranged from 0 to 35 cm. of wafer. The peristaltic contraction, the so-called systole, was usually recognized as a rapid raise to a single peak
I Fig. 4. Contraction staltic; waves 2 toward bladder. two which show increase, which of urine moving
I MwfOTE waves I and 4 move Note that nodular is presumably in front of
i and 3 are retraperiin normal direction it is only the latter introductory pressure caused by a pool peristaltic wave.
Fig. 5. Tracings from compression to 100 cm. of water (No. 2). Black line indicates time during which compression was applied. In upper tracing, from balloon above point of comamplitude decreases, and pressure finatly pression, waves become split, frequency increases, becomes permanently increased. Lower tracing-from balloon below point of compression frequency also increases initially, but then transfer of peristaltic waves is temporarily blocked. With the release of the compression, pressure decreases in the upper tracing and increases in the lower.
1336
Fig. 6. of
Enhijrning
Compression diastolic pressure
and
Weaver
of ureter in upper
to 100 tracing.
cm. of water Note abolition
followed by a somewhat slower fall in pressure. Its duration was 2 to 4 seconds and its peak value ranged from 50 to 180 cm. of water. It was frequently observed that the pressure wave started with a slow nodular pressure increase which lasted up to half a second, and which was followed by a more abrupt and vigorous increase in pressure (Fig. 3). The frequency of ureteral peristalsis was usually regular and ranged from 3 to 20 contractions per minute. The amount of urine transported past the catheter could only be estimated subjectively. It was observed, however, that urine was expelled along the catheter in each case. During high diuresis the frequency of the peristaltic waves was increased; .the nodular pressure increase at the beginning of systole (Fig. 3)
for
7.5 minutes gave of activity in lower
only slight tracing.
increase
was more pronounced and retroperista’itic waves were rare. Since the two recording balloons were 5 cm. apart, the direction and speed with which the peristaltic wave moved along the ureter could be determined. The peak or the start of the very abrupt raise in intraureteral pressure, as observed in some cases, served as reference points for such determinations. It was found that the peristaltic wave prior to compression moved with a speed of 3 to 5 cm. per second. The direction of the movement was generally toward the bladder, but retroperistalsis was frequently observed especially just after the catheter had been introduced. It could be provoked by stimulating the ureter mechanically beIow the balloons of the catheter. A retroperistahic wave showed a very abrupt increase in pressure
1338
Enhtirning
and
Weaver
though they might have become divided irl the upper tracing, If this was the case, one of the peaks in the upper tracing could be distinguished as being the one, preceding the peak of the lower tracing, with the same time interval as the undivided contraction of the upper tracing had previously preceded that of the lower tracing. In 6 of 23 compressions it was noticed that after 3 to 6 minutes every other peristaltic wave in the upper tracing was missing in the lower. This blocking could become more serious and only scattered waves would reach the lower balloon. Finally the ureter below the point of compression could become completely inactive for several min-
longer visible, the only alterations in pressure being those which were synchronous with the arterial pulse. In the lower tracing, which was from the lower balloon, changes could soon be recognized after compression had been applied. The introductory nodular rise in intraureteric pressure, if present prior to the compression, disappeared instantaneously (Fig. 3). The contractions in the lower tracing increased in frequency and decreased in amplitude just as they did in the upper tracing from the balloon above the point of compression. In the lower tracing the peristaltic contractions remained as single peaks even
Table II. Ureteral shown
within
activity parenthesis)
when
maximally
affected
55 (-30) 85 (01
by compression
(changes
1 2
11 53
50 100
5 (+5) 80 (+80)
3 4 5 6 7*
4 2 15 26 20
50 50 50 50 100
tl 45 70 90 cl
8 9
11 9
50 100
45 (+ZO) 85 (+60)
120 (0) 100 (-20)
125 (0) 110 (-15)
4 7% 25
50 100 100
20 (+15) 15 (+lO) 20 (+15)
85 (-5) 75 (-15) 60 (-30)
45 (-5) 40 (-10) 25 (-25)
13 14t
8 9
100 100
40 (+25) 90 (+75)
115 (0) 105 (-10)
15 16 17
1‘2 11 40
50 50 100
20 (+lO) 5 f-5) 60 (+50)
55 (-10) 40 (-25) 60 (-5)
65 (-10) 60 (-15) 45 (-30)
24 (+14) 14 (+4) 17 (+7)
18 19 20
8 31 33
50 100 100
5 (+5) 8CI (+80) 80 (+80)
75 (-10) 85 (01 85 (01
95 (0) 105 (+-lo) 115 (+ZO)
19 (+lO)
12 63
50 100
5 (+5) 50 (+50)
55 (-5) 75 (+15)
65 (-20) 80 (-5)
25 (+19) 25 (+19)
25 (+ZO)
80 (-24)
10 ii
10 23 15 100 *Upper ureter drained. $After intravenous saline infusion. $Pe&taLsis disappeared in both tmcings.
(0) (+45) (+70) (+90) (01
85 65 80 95 125
65 (-5) 60 (-10)
(-30) (-50) (-35) (-20) (+lO)
95 85 90 75 125
110 100
ilium
(-10) (-20) (-15} (-30) (+ZO)
(0) (-10)
180 (0)
16 (+7) 16 (+7) 14 11 15 20 5
(+7) (+4) (4) (+13) (-2)
12 (-5) 25 (+8) 22 (+14) 20 (+12) 18 (+lO) 4 (-3) -
20 (All) 20 (+ll)
35 (+32)
vohme Number
90 8
utes. Its internal pressure would remain at the low value which had been recorded in the interval between contractions. Compression No. 7 which followed drainage of the upper ureter gave a result which was completely different from any of the other experiments including those in the same dog. Although the compression was 100 cm. of water no increase in diastolic pressure was seen in the upper tracing nor was there any increase in frequency. All peristaltic waves showed an abrupt pressure increase and they never split. As was so frequently seen during the other compressions, there was interference with the transfer of the peristaltic wave. Several of the contractions seen in the upper tracing were missing in the lower. Instead, series of contractions could spontaneously occur in the lower tracing and these could more or less completely be transferred upward. Comment
Recording of intraureteric pressure in dogs with an electromanometer has previously been reported.13s1s Weinberg and Siebens14 found that the peak pressure during a peristaltic contraction was no more than 10 to 20 mm. Hg. This is only about one-fifth of the value reported in the present study. The difference in method may be the explanation for this discrepancy. Weinberg and Siebens used an open catheter for transmission of pressure from ureter to transducer, whereas in the present study a flaccid liquid-containing balloon was used as an intermediate pressure transmitter from ureter to catheter, When a pressure increase is transmitted via a catheter to a transducer chamber, liquid moves in through the catheter to the chamber as the membrane of the latter is displaced. During a ureteral contraction urine will be pushed away and it will then be the mucosa of the ureter which moves into the opening of the catheter. Although most transducers have a low volume displacement, the movement of the mucosa cannot be disregarded. It will not move into the catheter as readily as a liquid would
lntraureteric
pressure
and
compression
)339
and, therefore, falsely low pressures may be recorded with an open catheter. However, erroneous results may also be obtained with the balloon-covered catheter. The errors inherent with such a catheter have been clearly reviewed by Mead.lg He points out that if the balloon is surrounded by a uniform pressure, the pressure inside the balloon is the same as that outside as long as the intervening rubber wall is unstretched. If, however, the balloon is exposed to a nonuniform pressure, that whicli is recorded will depend upon the degree of inflation of the balloon. At small balloon volumes it will approximate the highest pressure. In this study the balloon was flaccid and, thus, had an unstretched wall. The bailoon was of a very small size which reduced the nonuniformity of the pressure surrounding it. It, therefore, seems unlikely that the pressures recorded were erroneously high. The division of the peristaltic contraction wave into two or three peaks has been described previously, lo1 I1 but the phenomenon has not been interpreted. The fact that two to three peak waves were frequently seen above but never below the point of compression would imply that they had something to do with collection of urine above this point. It seems possible that in the case of a double peak the first top was caused by the pool of urine being pushed in front of the contraction wave and the second top by the ureteral contraction, itself. In Fig. 6 it may be noted that in the beginning of the compression it is only the peristaltic waves, moving in the normal direction toward the bladder and which thus may be expected to move urine in front of them, which are split into two peaks. The retroperistaltic \vaves are all single peaked. It also seems likely that the nodular pressure increase so often seen to precede the contraction wave proper, but consistently disappearing in the lower tracing immediately after compression has started, is caused by the urine which is pushed in front of the peristaltic contraction wave. Compression of the ureter was never seen
1340
Enhtirning
and
Weaver
I MINUTE Fig. 8. Compression
to 100 cm. of water for 20 minutes. In this experiment a draining catheter had been inserted into the upper ureter. Upper tracing showed no splitting of peristaltic waves, no increase in frequency, no increase in diastolic pressure, and no change of amplitude. The compression interfered with transfer of contractions to lower balloon. However, immediately after release of compression normal peristalsis was reestablished.
to promote stronger contractions, but it almost consistently stimulated increased frequency. This observation confirms that of Sleator and Butcher.13 These investigators demonstrated that ureteral obstruction, infusion of saline into the ureter or expansion of a balloon in the ureter, almost immediately leads to increased frequency. Increase in the volume of urine to be transported seems to be the trigger mechanism to more frequent contractions.zo Compression No. 7 of this study (Fig. 8) which did not result in increased diastolic pressure, since the upper ureter was drained, and which did not affect the frequency would seem to substantiate this concept. The increased frequency, observed in the nondrained ureter, may be of importance as a means of securing transport of urine past a moderate ureteral compression, thus protecting against stasis of urine which eventually might increase pelvic pressure. The finding of ordinarily continued, but
occasionally interrupted, transportation of urine past an area of compression to 50 cm. of water, and complete blockage when compression was raised to 100 cm. of water, would be more meaningful clinically if it were known how much intraureteric pressure is increased because of compression during the last months of pregnancy. Direct recordings of pressure in the lower ureter of the pregnant woman in the erect position have not been performed yet, and we can only roughly calculate how much intraureteral pressure might be increased because of compression by the engaged fetal head. There is reason to believe that in the erect position ligaments offer very little support to a pregnant uterus at term with the head engaged. Therefore, the weight of the uterus which at term is about 5,000 grams is resting on a ring-shaped area at the pelvic inlet. With the assumption that this area is 2 cm. wide and has a radius of 6 cm. the 5,000 grams weight would be distributed
lntraureteric
over a surface of approximately 75 cm.z The pressure would thus be about 65 grams per centimeter2 or 65 cm. of water. With this figure even support of the uterus by the ring-shaped area in the pelvic inlet is assumed. More likely, however, the weight of the uterus is not quite evenly distributed over this area. Thereby the ureter may be protected, but there is also a possibility that its intraluminal pressure may be increased with more than 65 cm. of water. If this calculation is correct and if the human ureter during pregnancy reacts as does the nonpregnant dog’s ureter, it would seem from this study that the transfer of urine from the kidney could become temporarily completely blocked. However, the cnmpression of the ureter will not be equal on both sides and it may also be assumed to be intermittent. When the pregnant woman changes position, and especially when she lies down, the ureter may be relieved from its compression. The fact that the ureter of a pregnant woman has much lower tonus, and therefore is dilated, makes it capable of collecting a large volume of urine without a critical increase of intrapelvic pressure. At night, when the ureter is decompressed, the collected urine will have free entrance to the bladder which may contribute to nocturia. It may be noted, however, that even in the supine position diuresis may be disturbed. Hendricks and Barne? found that urinary output of a pregnant patient in the last trimester is considerably greater with the patient lying on the side than on the back. These investigators felt that this was at least partly caused by relief from ureteral compression which could occur when the patient was lying on the side. Dilatation of the ureter may thus be regarded as a safeguard against rise of intrapelvic pressure caused by ureteric compression. However. if the urinary output is high and if the compression is long lasting, the ureter may become filled to its capacity and its intraluminal pressure may then be expected to rise just as it did in several of the dogs. In the pregnant woman at term uninterrupted standing may possibly evoke this
pressure
and
situation which would with kidney function.zz-zS
compression
seriously
1341
interfere
Summary Ten dogs were studied to ascertain whether or not the ureter, when compressed to pressures near the normal systohc value, is able to react with increased systolic pressure or with other means of coping with an increased resistance caused by compressing tumor or pregnant uterus. The lower ureter was subjected to a compression of 50 or 100 cm. of water over a 1 cm. portion, above and below which intraureteric pressure was simultaneously recorded. Twenty-three compressions were IJcrformed. In one case the upper ureter was drained prior to the compression. Prior to compression. 1. Urine was expelled along the catheter in each case. 2. Pressure between contractions was low and ranged from 0 to 35 cm. of water. 3. Contractions lasted 2 to 4 seconds and increased pressure to 50 to 180 cm. of bsater. 4. The peristaltic waves traveled at S to 5 cm. per second and with a frequency ranging from 3 to 20 contractions per minute. 5. Retroperistaltic waves were frequently seen and could be provoked by mechanical stimulation of lower ureter. During compression. 1. No urine was expelled when the ureter was compressed to 100 cm. of water. 2. Urine continued to be expelled in 8 of 11 compressions to 50 cm. of water. 3. Pressure between contraction waves increased to 45 to 90 cm. of water in 11 cases. 4. Contraction waves above the compression were split, increased in frequency, and decreased in peak value. None of these changes were seen in the drained ureter. 5. Contraction waves below cnmpression could completely disappear. Thus only with an increase in frequency can the ureter cope with an augmented resistance. It is felt, however, that the relaxation of the ureter in pregnancy may be a safeguard against increase in intrapelvic pressure. The ureter may act as a low pressure reservoir which may empty when compression is released.
1342
EnhSrning
and Weaver
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1.
2. 3.
4.
5. 6. 7.
8.
9.
10.
11.
Robertson, H. E.: Hydronephrosis and pyelitis of pregnancy, Philadelphia, 1944, W. B. Saunders Company, p. 5. Tram, H. F., &Lane, C. M., and Kuder, A.: Sum. Gvnec. & Obst. 64: 51. 1937. Crabtree: E. G.: Urologicai diseases of pregnancy, Boston, 1942, Little, Brown, & Company, pp. 115-120. Eastman, N. J., and Hellman, L. M.: Obstetrics, ed. 12, New York, 1961, AppletonCentury-Crofts, Inc., pp. 254-257. Fainstat, T.: AM. J. OBST. & GYNEC. 87: 486, 1963. Kumar, D.: AM. J. OBST. & GYNEC. 84: 1300, 1962. Hundley, J. M., Jr., Walton, H. J., Hibbitts, J. T., Siegel, I. A., and Brack, C. B.: AM. J. OBST. & GYNEC. 30: 625, 1935. Greenhill, J. P.: Obstetrics, ed. 12, Philadelphia, 1960, W. B. Saunders Company, p. 100. Graham, J. B., Sotto, L. S. J., and Paloucek, F. P.: Carcinoma of the cervix, Philadelphia, 1962, W. B. Saunders Company, p. 66. Kiil, F.: The function of the ureter and renal pelvis, Philadelphia, 1957, W. B. Saunders Company. Davis, D. M., Zimskind, P. D., and Paquet, J. P.: J. Ural. 98: 150, 1963.
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