Function of the Collecting Ducts
By KARL J. ULLRICH, M.D.
Urine was sampled from microcatheters situated at different levels of the collecting ducts
of golden hamsters. Appropriate analyses provided data concerning the function of the
collecting ducts with respect to concentrating and acidifying the urine. The conclusion
is reached that the collecting ducts serve 2 functions: a passive one, i.e., the back-diffusion
of water and urea and an active one, i.e., the exchange of sodium for hydrogen ions and
the formation of ammonia.
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HEIDENHAIN1 la in 1874 injected indigo
carmine into intact animals and found
a strong concentration of color in the collecting ducts. His explanation was that there is
relatively more urine in the collecting ducts
and that some precipitated dye is collected by
coagulation in a manner analogous to sand
being swept along by a stream. He attributed
no special function to the cells of the collecting ducts because of their clear appearance.
This interpretation was accepted for 70 years.
In 1949 Vimtrup,2 in the laboratory of Bodil and Knut Schmidt-Nielsen, repeated experiments with dyes on Heteromyidae whose
collecting ducts are very long and a good subject for experimental study. He concluded
that the urine becomes concentrated as it flows
through the collecting ducts. In 1931 Hargitay
and Kuhn3 published their countercurrent
hypothesis, showing by experiments performed in conjunction with Wirz,4 that the
urine was concentrated in the collecting ducts.
To obtain more information about the function of collecting ducts, Hilger, Kliimper,
Eigler, Pehling and Ullrich5-8 catheterized the
collecting ducts of golden hamsters, whose
papillae are easily accessible from the renal
pelvis. The experimental procedure was as
follows: 2 polyethylene microcatheters were
passed from the renal pelvis into 2 collecting
ducts, the tips reaching different levels. Both
samples of urine which were obtainied in this
way were analyzed with respect to the depressions of the freezing point and the concentrations of inulin, sodium, and potassium.
The results are plotted in figure 1. In 33
cases, the concentration of inulin in urine
from the superficially placed catheter averaged 1.5 times that from the deeper one. In a
second series of animals with higher urinary
osmotic pressure, the mean increase was threefold. If it is assumed that the increase in inulin concentration is due to the reabsorption of
water, the results of both series indicate that
between one-third and two-thirds of the water
flowing into the portions of the collecting
ducts under consideration is reabsorbed.
If water alone is reabsorbed from the fluid
of the collecting ducts, the increase in osmotic
pressure ought to parallel the increase in the
concentration of inulin. But (fig. 2), such
parallelism was not observed: the real osmotic
pressures increase with much less of a slope.
From this discrepancy one can conclude that
some solutes must be reabsorbed too, thereby
making the osmotic pressure of the reabsorbed
solution equal to about two-thirds of that of
the solution flowing into the corresponding
segment of the collecting ducts.
In other experiments, Kliimper, Ullrich,
and Hilger6 measured the concentrations of
inulin alnd urea in samples obtained from
microcatheterization of collecting ducts. In all
eases the inerease in the concentration of inulin exceeded that of urea. The ratios of the
rate of increase in the concentration of urea
to the rate of increase in the concentration of
inulin varied from 0.37 to 0.97, with an average of 0.65. These data indicate that the eon-
From the Physiological Institute, University of
Gottingen, Gottingen, Germany.
Dr. Ullrich is presently a Research Associate, Department of Zoology, Duke University, Durham, N. C.
Circulation, Volume XXI, May 1960
869
I TTLLRICH
870
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li
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Figure 1
Relative changes in the concentrations of inulin in the urine within the collecting duct,
and the corresponding reabsorption of water. The data illustrated on the right side of
the figure are from animals excreting a more concentrated urine than those on the left.
On the abscissa are plotted the distances of sampling points from the tip of the papilla.
The straight lines represent the values of the simultaneously gained samples. Data taken
from Hilger, Kliimper and Ullrich.5
centration of urea in the reabsorbed solution
is approximately half the concentration of the
fluid flowing into the particular segment of
the collecting duct from which samples were
obtained.
What changes occur in the electrolytes during the passage of urine through the collecting
ducts? On the average, the increases in the
concentrations of potassium parallel the increases in the concentrations of inulin.5 This
supports the view that potassium is concentrated only by reabsorption of water in the
collecting ducts of the inner medullary region.
The concentrations of sodium in the urine,
however, fall as the urine passes through the
collecting ducts.5 As may be seen in figure 3,
there is a steep slope, with high values for
concentration in the outer medullary region.
This fact indicates that a great deal of water
is reabsorbed from the collecting ducts of the
cortex and the outer medulla. The sodium
concentrations are very low at the papillary
tip. Thus, sodium must be reabsorbed from
the collecting ducts. We may then conclude
that the collecting ducts can regulate the excretion of sodium by the kidney.
But how can this drop in the concentration
of sodium be reconciled with the coincidental
rise in the osmotic pressure of urine in the
same region? Simultaneous measurements of
the concentrations of inulin and ammonium by
Ullrich, Hilger, and Kliimper8 indicate (fig.
4) that ammonium increases much more than
inulin. Therefore, we may conclude that ammonium ions are secreted into the collecting
ducts. In connection with this observation,
it is interesting to note that Richterich-van
Baerle, Goldstein, and Dearborn9 have deCirculation, Volume XXI, May 1960
L-I
FUNCTION OF THE COLLECTING DUCTS
871
Wasserruickresorption ous den Summelrohren
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"5mm
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Urinkonzentrationsveronderufgef
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im Verlouf der Somnmelrohrp,ossoge
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Figure 2
Changes in the osmotic pressure of urine along the course of the collecting duct. The
data used for the left side of the figure were calculated from the freezing-point depression
of urine obtained from the deeper level and the respective concentrations of inulin in
urine from both levels. This hypothetic figure would be expected if only water were
reabsorbed. The observed increases in osmotic pressure (right) are less. Data taken from
Hilger, Kliimp,er and Ullrich.5
iq/l, _
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Figure 3
Changes in the concentrations of sodium during the passage of urine through the
collecting duct (26 experiments on golden hamsters). On the abscissa is plotted the
distance of the sampling point from the tip of the papilla. b. Changes in the concentrations of potassium during the passage of urine through the collecting duct (23 experiments). (Republished by permission of Pfiiger's Archiv fur die gesamte Physiologie des
Menschen und der Tiere.5)
a.
Circulation, Volume XXI, May 1960
UlTLRICH
872
>NH4 +
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Figure 4
Changes in the concentration of ammonia in urine during the passage through the collecting duct compared with the changes in the concentration of inulin and in the osmotic
pressure in the same sarmples (4 representative experiments). Data taken from Hulger,
Kliimper and Ullrich.5
scribed a high degree of activity of glutaminase I in the inner zone of the renal medulla
of dogs and rabbits. Moreover, as may be seen
in figure 5, acidification of urine within the
collecting ducts was demonstrated by a decrease of pH.7 These observations were recently confirmed by Gottschalk'0 and Giebisch,1" who have also shown that acidification
can take place in the proximal and distal convolutions. The present data indicate that there
is an exchange of sodium ions for hydrogen
ions and a secretion of amumonia in the collecting ducts.
The findings by the stop-flow method'12-5
in accord with our results as far as the
reabsorption of sodium and the secretion of
hydrogen ions and ammonia are concerned.
However, a discrepancy exists with respect to
the site of secretion of potassium. According
to the stop-flow method, potassium is secreted
at the same site as hydrogen ions and ammonia. However, our results indicate that potassium is not secreted in the collectinig ducts of
the inner medullary region, but that secretion of potassium may occur at a site higher
up in the collecting ducts.
are
Circulation, Volume XXI, May 1960
873
FUNCTION OF THE COLLECTING DUCTS
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54
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Figure 5
The pH of urine drawn simultaneously from the collecting duct at different distances
from the tip of the papilla. The graph on the left represents values of samples withdrawn
without special precautions. The values for the graph on the right were measured at a
carbon dioxide tension of 40 mm. Hg. The values at abscissa point 0 are values from
the other (unexposed) kidney. (Republished by permission of Ergebnisse der Physiologie,
Biologischen Chemie uand Experimentellen Pharmakologie.7a)
To summarize, the collecting ducts seem to
have 2 functions: (1) a passive one, i.e., the
back-diffusion of water and urea, and (2) an
active one, i.e., the exchange of sodium iolns
for hydrogen ions and the formation of ammionia. Both functions, passive and active,
seem to operate independently. It is partieularly surprisinog that the cells of the collectilng ducts, which are exposed to enormous
changes in the concentrations of electrolytes
and urea, and are threatened by an inadequate
supply of oxygen and essenitial nutrients as a
consequence of countercurrent diffusion, are
entrusted with such essential functions as the
exchange of sodium and hydrogen and the secretion of ammonia. 7a
Circulation, Volume XXI, May 1960
References
1. HEIDENHAIN, R.: Mikroskopische Beitriige zur
Anatomie und Physiologie der Nieren. Areh.
mikr. Anat. 10: 1, 1874.
la. -: Versuche fiber den Vorgang der Harnabsonderung. Pfliugers Arch. ges. Physiol. 9: 1,
1874.
2. VIMTRUP, B.: Histological examinations of kidneys of Heteromyidae. Scandinav. J. Clin. &
Lab. Invest. 1: 339, 1949.
3. HARGITAY, B., AND KUHN, W.: Das Multiplikationsprinzip als Grundlage der Harnkonzentrierung in der Niere. Ztsehr. Elektrochem.
55: 539, 1951.
4. WIRz, H., HARGITAY, B., AND KUHN, W.: Lokalisation des Konzentrierungsprozesses in der
Niere durch direkte Eryoskopie. Helvet.
physiol. et pharmaeol. acta 9: 196, 1951.
5. HILGER, H. H., KLUMPER, J. D., AND ULLRICH,
874
ULLRICH
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K. J.: Wasserrflckresorption und Ionentransport durch die Sammelrohrzellen der Saugetierniere. Pflugers Arch. ges. Physiol. 267:
218, 1958.
6. KLfiMPER, J. D., ULLRICH, K. J., AND HILGER,
H. H.: Verhalten des Harnstoffs in den Sammelrohren der Saugetierniere. Pfiigers Arch.
ges. Physiol. 267: 238, 1958.
7. ULLRICH, K. J., EIGLER, F. W., AND PEHLING, G.:
Sekretion von Wasserstofflonen in den Sammelrohren der Siaugetierniere. Pfluigers Arch.
ges. Physiol. 267: 491, 1958.
7a.-: Das Nierenmark Struktur Stoffwechsel und
Funktion. Ergebn. d. Physiol. 50: 433, 1959.
8. -, HILGER H. H., AND KLt-MPER, J. D.: Sekretion von Ammoniumionen in den Saminelrohren
der Saugetierniere. Pfliigers Arch. ges. Physiol.
267: 244, 1958.
9. RICHTERICH-VAx BAERLE, R., GOLDSTEIN, L., AND
DEARBORN, E. H.: Ammonia production in the
collecting ducts of nmaminalian kidneys. Nature
178: 698, 1956.
10. GOTTSCHALK, C. W., LASSITER, W. E., AND MYLLE,
M.: Localization of urine acidification in the
mammalian kidney. Am. J. Physiol., in press.
11. GIEBISCH, G., WINDHAGER, E. E., AND PITTS,
R. F.: Mechanism of urinary acidification. In
Proceedings of the International Symposium on
the Biology of Pyelonephritis. Bostoni, Little,
Brown & Co., in press.
1 2. MALVIN, R. L., WILDE, W. S., AND SULLIVAN,
L. P.: Localization of niephron transport by
stop flow analysis. Ain. J. Physiol. 194: 135,
1958.
1 3. PITTS, R. F., GuRD, R. S., KESSLER, R. HI., AND
HIERHOLZER, K.: Localization of acidification
of urine, potassium anid ammonia secretion
and phosphate reabsorption in the nephron of
the dog. Am. J. Physiol. 194: 125, 1958.
14. WILDE, W. S., AN D MALVIN , R. L.: Graphical
placement of tranisport segments along the
nephron from urine concentration pattern developed with stop flow technique. Am. J.
Physiol. 195: 153, 1958.
13. KESSLER, R. H., HIERHOLZER, K., GURD, R. S.,
AND PITTS, R. F.: Localization of diuretic action of chlormerodrin in the nephron of the
dog. Am. J. Physiol. 194: 540, 1958.
The Animal that Fits
In 1926, Marshall, browsing through comparative anatomuy, discovered that a number
of fishes had been described which possessed purely tubular kidneys. This fact, of course,
immediately evoked Marshall's interest in fish urine. Unfortunately, aglonierular fishes
were rather rare, but we happened to have one species, the goosefish, at Salisburv
Cove ...
Work on the aglomerular fishes had been undertaken independentlv by J. G. Edwards
in the Naples' laboratory, and within a short time it was clear that this purely tubular
kidney, which does not even possess a significant arterial blood supply, but is perfused
entirely by venous blood fromi the renal portal vein and at a pressure which is probably
below the osmotic pressure of the plasma proteins, can excrete all the ordinary urinary
constituents
So, by 1930, the question of tubular excretion was answered in the affirmative. But, as
Richards said in the discussion when Marshall read a paper at Woods Hole on the
aglomerular fish, "At last he has found an animal that fits in with his theory."-H. W.
Smith. Lectures on the Kidney. Lawrence, Kansas, University of Kansas Press, 1943,
p. 73.
Circulation, Volume XXI, May 1960
Function of the Collecting Ducts
KARL J. ULLRICH
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Circulation. 1960;21:869-874
doi: 10.1161/01.CIR.21.5.869
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