Intrarenal blood flow distribution in the desert quail - 2nd Chance

AMERICAN JOURNAL OF P~yt310~00~

Vol. 231, No. 4, October 1976. Printed in U.S.A.

Intrarenal blood flow distribution in the

desert quail following salt loading

ELDON J. BRAUN

Department of Physiology, College of Medicine, University of Arizona, Tucson, Arizona 85724

BRAUN, ELDON J. Intrarenal blood flow distribution in the desert quail following salt Loading. Am. J. Physiol. 231(4): 1111-1118. 1976. -The total-kidney glomerular filtration rate (GFR) falls when birds are salt loaded. This fall in GFR is caused by glomerular intermittency. The nephrons that stop filtering are small, surface nephrons without loops of Henle. Larger nephrons with loops of Henle in the deeper regions of the kidney continue to filter during salt loading. Microfil casts were made of the renal microvasculature of the desert quail, Lophortyx gambelii, in an attempt to determine at what points intrarenal blood flow is regulated to cause glomerular intermittency. Casts of the renal vasculature were made in quail that were hydrated and in quail that were salt loaded. The results indicate that the small, surface nephrons stop filtering during salt loading because of a vasoconstriction at the level of the afferent arterioles of these nephrons. At the same time, blood flow is maintained to the large nephrons with loops of Henle. Reducing GFR at the expenses of excreting wastes can be viewed as a mechanism to conserve body water during periods of water deprivation.

comparative renal physiology; avian renal physiology; Lo- phortyx gambelii; intermittent nephron function; water con- servation

BIRDS WITHOUT FUNCTIONAL salt glands, whensubjected to dehydration or salt loading, can respond with several homeostatic mechanisms in attempts to conserve body water. These mechanisms include allowing the plasma osmolality to increase, producing a more concentrated urine, and reducing the glomerular filtration rate.

By not excreting all ions that would be excreted under conditions of normal hydropenia and allowing plasma osmolality to slowly increase during periods of stress, birds can conserve valuable body water. The plasma osmolality of birds subjected to dehydration or salt loading increases with time (5, 8). Such increases in plasma osmolality can be marked. When desert quail were salt loaded, the plasma osmolality reached 500 mosM (5). McNabb (12) also reported plasma osmolality values much in excess of 300 mosM for three species of quail. From these data it is apparent that birds are more tolerant than mammals to fluctuations in plasma osmolality and use it as a mechanism to compensate for dehydration rather than use valuable body water to excrete ions.

Production of a more concentrated urine during periods of stress is an obvious mechanism for conserving body water. It has been assumed that birds without salt

glands are limited in their capacity to excrete ions in excess of water to control the osmolality of body fluids. This assumption was based on data which indicated that most birds without salt glands could elaborate a urine only 2-2.5 times as concentrated as the plasma (5). The only exception is a salt marsh Savannah sparrow which has been reported to produce a urine 4 times as concentrated as the plasma (14). Some of the low urine- to-plasma osmolar ratios may be due to high plasma osmolalities. However, recent data (13; unpublished data) indicate that conventional urine-to-plasma osmolar ratios do not give a true indication of the quantities of ions excreted by birds. The recent data indicate that uric acid and urate nitrogen excretion aid in the renal excretion of cations. It appears that variable quantities of ions can be excreted with the uric acid depending on the composition of the diet (13; unpublished data). These ions are excreted in a precipitated form with uric acid and do not contribute to the osmotic activity of the urine. This permits birds to conserve that quantity of water that would otherwise be required to hold these ions in solution.

When birds are artificially dehydrated by salt loading, the total-kidney glomerular filtration rate (GFR) falls (4, 7). The fall in GFR is caused by a reduction in the number of filtering nephrons and not a reduction in filtration rate by all the nephrons. The reduced GFR allows these birds to conserve water at the expense of excreting waste. Under these conditions the plasma osmolality would slowly increase. However, as pointed out above, birds appear to be more tolerant of variations in plasma osmolality than mammals.

The nephrons within the avian kidney that stop filtering during periods of water deprivation are small nephrons without loops of Henle situated in the superficial regions of the kidney. Because of their close resemblance to nephrons found in reptilian kidneys, these nephrons are called reptilian-type nephrons (9). With their simple structure and attachment to collecting ducts, the RT nephrons do not contribute directly to the countercurrent multiplier mechanism by which the avian kidney can elaborate a urine hyperosmotic to the plasma. Nephrons with loops of Henle are situated in the deeper regions of the avian kidney. Because of their close resemblance to nephrons found in mammalian kidneys, these nephrons are called mammalian-type (MT) nephrons (9). The MT nephrons are arranged in a parallel fashion with vasa recta and collecting ducts and

1111

1112 E. J. BRAUN

appear to function in a countercurrent multiplier sys- tem which allows the avian kidney to elaborate a urine hyperosmotic to the plasma. These larger, more com- plex nephrons continue to filter when birds are dehydrated (5).

This glomerular intermittency during stress in birds is probably caused by redistributions of intrarenal blood flow. The present studies were undertaken in an attempt to determine how this might occur within the kidney of the desert quail, Lophortyx gambelii. Intra- renal blood flow distribution patterns were studied in normal hydrated quail and in quail that were dehydrated by salt loading. Attempts were made to determine at what points in the renal microvasculature blood flow is regulated to reduce the number of filtering RT nephrons. The results of these studies indicate that this regulation of intrarenal blood flow takes place at the level of the afferent arterioles of the RT nephrons. The redistribution of blood flow that follows results in a decrease in the total-kidney GFR during periods of osmotic stress.

METHODS

Animals and operative procedures. Desert quail, Lophortyx gambelii, were used as experimental animals. The quail weighed from 144 to 162 g (mean weight, 156 g). They were trapped in their native habitat in the vicinity of Tucson, Arizona (Trapping Permit No. 60 from Arizona Game and Fish Department) and were main.tained in an outside aviary exposed to natural environmental conditions. Eight birds were used in the present study. In captivity the birds had free access to a cracked grain mixture and green fodder and were allowed water ad libitum. The birds were anesthetized with Equi-thesin (Jensen-Salsbury, Kansas City, MO.) (3 ml/kg) prior to surgery. A 2% lidocaine solution was used as a local anesthetic during the operations. During the operative procedures and experiments, the birds were restrained by taping their legs and wings to a specially designed bird board. The left brachial vein and artery were cannulated with PE-10 polyethylene tubing for intravenous infusions and collection of arterial blood samples. Ureteral urine was collected by exteriorizing the ureters and cannulating them with PE-50 polyethylene cannulas as previously described (5). Dead space in each ureteral cannula was 18-20 ~1. A PE-10 polyethylene cannula was placed in the left sciatic artery and advanced in a retrograde fashion toward the posterior renal arteries. The silicone rubber injections were made through this cannula.

Intrarenal bZood flow patterns. The intrarenal blood flow distribution within the kidney of the desert quail was studied by making casts of the renal vasculature with a low-viscosity silicone elastomere. The casts were made after birds had been subjected to different physiological manipulations which previously had been shown to change the rates at which the individual nephrons filter. The silicone elastomere used in these studies was Microfil (Canton Biomedical Products, Boulder, Colo.). Microfil is ideally suited for the infusion of microvascular networks (2, 3). The viscosity of this elastomere can

be adjusted to that of systemic blood and the elastomere is not miscible with blood. This eliminates the need to wash out the tissue before infusions are made. The Microfil used in the present studies consisted of one part Microfil MV-112 and three parts MV diluent to which 3% by volume of dibutyltin dilaurate catalyst was added. The catalyst was added just before the Microfil was infused into the renal microvasculature by way of the cannula inserted into the sciatic artery. The infusions were made at a constant pressure of 110-115 mmHg for a period of 5 min. The average systemic arterial blood pressure of the desert quail as measured from the sciatic artery is 112 mmHg (6). The infusion pressure was monitored by a Statham P23Gb pressure transducer connected to one arm of a four-way valve. During the 5-min infusion periods, the renal vein was opened to allow drainage from the kidney. After the completion of the infusions, both the renal vein and the infusion cannula were clamped. The birds were then given an overdose of anesthetic. The silicone rubber was allowed to cure overnight before the kidneys were dis- sected free of the synsacrum. The Microfil mixture used in the present studies began to “setup” within 15 min from the time the catalyst was added.

The kidney tissue was rendered transparent (cleared) so the Microfil casts of the vasculature could be studied. The clearing procedure was as follows: the tissues were dehydrated by passing them through a series of ethyl alcohols of increasing concentrations starting with a 25% solution. After the absolute alcohol step, the tissues were placed in a mixture of equal parts toluene and a Cargille immersion oil (R. P. Cargille Laboratories, Cedar Grove, N. J.) with a refractive index of 1.568. For the final clearing the tissues were placed in a pure solution of the Cargille immersion oil. Methyl salicy- late, which is commonly used to clear mammalian renal tissue (2) and has a refractive index of 1.522, does not adequately clear avian renal tissue.

The renal microvasculature of the desert quail was studied in birds that were subjected to two physiological manipulations. One group of four birds received only an intravenous infusion of 2.5% mannitol (control studies). A second group of four birds received the same 2.5% mannitol infusion followed by an infusion of 1 M NaCl (salt-loading studies). All infusions were given at the rate of 0.4 ml/kg per min. In the control mannitol studies, four lo-min clearance periods were taken before the renal microvasculature was infused with Microfii. In total, each bird received at least 140 min of the 2.5% mannitol infusion. In the salt-loading studies, four lo- min control clearance periods (2.5% mannitol infusion) were taken before the salt load was started. The salt load consisted of a 1 M NaCl solution infused at the same rate as the control solution. The salt loading was continued until 35 meq of NaCl per kg body wt had been infused. After the infusion of the 35 meq of NaCl, the renal microvasculature was infused with Microfil.

CZearance studies. Glomerular filtration rates were estimated as inulin clearances using inulin carboxyl- 14C. A priming injection of 1 ,uCi was given and the blood level was maintained by a constant infusion of 0.06 ,&i/kg per min; 40 min were allowed for equilibra-

EFFECTS OF SALT LOAD ON RENAL BLOOD FLOW IN DESERT QUAIL 1113

tion of the marker before the first clearance period was 160 - 0 Urine flow

taken. Clearances were determined separately for each 140 - 0 GFR

kidney. All collection periods were 10 min in length. 2 120- 7

0

Arterial blood samples of 0.15-0.2 ml were taken every z 100 I, 1 4 1 I ” 0

20 min. + 80- 9-

8 li

1-l ” - 60- 9- P i

RESULTS

Renal function prior to Microfil infusion. In all ex- 20- periments, total-kidney GFR and urine flow were mea- 0

sured before the renal vasculature was infused with Microfil. The data on GFR and urine flow are listed in

NaCl infused mEq/Kg Body Weight

Table 1. The GFR and urine flow for the birds that FIG. 1. Glomerular filtration rate and urine flow during sodium

chloride infusion. Values are expressed as percents of average value

received only the 2.5% mannitol infusion (control groun) for three to four control periods in same animal before start of

were significantly (P < 0.001) higher than the GI?R and sodium chloride infusion. Data are from four birds. For both GFR

urine flow measured previously for the desert quail and urine flow, each point represents mean of four determinations.

under similar conditions (5). The GFR was 138% and the Vertical lines above and below each point represent standard errors.

urine flow 120% of the previously measured value. The mean GFR and urine flow measured for birds during control periods prior to salt loading were also significantly (P < 0.001) higher than the previously published values. However, the GFR and urine flow during the control periods before salt loading did not differ significantly from the GFR and urine flow of the birds that received only the 2.5% mannitol infusion in the present studies.

The GFR and urine flow are plotted against the sodium chloride infusion in Fig. 1. The GFR and urine flow are plotted as percent of control values with each bird serving as its own control. The GFR and urine flow decreased to about 60-65% of control when about 7 meq NaCl per kilogram body wt were infused. However, both the GFR and urine flow shortly returned to control levels. A similar early depression of the GFR and urine flow occurred in an earlier study on desert quail (6). However, the decreases were less marked. After a re- turn to control levels in the present study, the GFR began and continued to fall as the salt load increased. By the time 35 meq NaCl per kilogram had been infused, the GFR had fallen to 35% of the control level. It was at this point that the renal vasculature was infused with Microfil. The urine flow did not parallel the decrease in GFR. In fact the urine flow remained at or near the control level in spite of the fall in GFR and did not fall below control levels until 35 meq NaCl per kilogram were infused. Apparently increasing amounts of the filtered water were rejected and excreted. This was probably due to an osmotic diuretic effect caused by the sustained infusion of NaCl.

Avian renal anatomy. Before describing the results of the Microfil studies, a brief review of the anatomy of the avian kidney is given. A more detailed description of the

anatomy of the avian kidney appeared in an earlier publication (5).

The avian kidney does not resemble the mammalian kidney in external morphology. Externally the avian kidney does not exhibit the typical “bean” shape of the mammalian kidney but it is an elongated organ flat- tened in the dorsoventral aspect. Moreover, the internal gross morphology of the avian kidney is quite different from that of the mammalian kidney. The zonation of the cortical and medullary tissue that occurs in mammalian kidneys is not seen within the avian kidney. The cortical tissue where the RT nephrons are located can be seen to extend into the inner areas of the avian kidney, areas analogous to the medullary zone of the mammalian kidney. However the medullary areas of the avian kidney (medullary cones) contain the same elements as found in the renal medulla of mammals.

As is the case for most birds, arterial blood is con- veyed to each kidney by three renal arteries in the desert quail. The anteriormost of the renal arteries arises directly from the aorta and supplies the anterior division of the kidney. The middle and posterior renal arteries do not originate from the aorta but as branches from the sciatic artery as it crosses the kidney on its way to the leg. In those mammalian kidneys where lobes are arranged regularly around the renal pelvis, there is a strict lobular pattern to the arterial supply. The interlo- bar arteries are easily identifiable as they run along the calyxes and between the pyramids. In birds the early internal ramifications of the renal arteries are less clearly defined. This leads to a lack of a distinct pattern to the arterial supply to the MT nephrons. The absence of an ordered arrangement of the lobes within the avian kidney is responsible for this lack of a clear pattern in the early arterial supply to the MT nephrons (Fig. 2). On the other hand, a very regular pattern is formed by the arterial supply to the RT nephrons. Four arteries enter each cortical lobule where the RT nephrons are located, forming a very symmetrical pattern about the central efferent vein (Fig. 2). These arteries I shall refer to as intralobular arteries. The afferent arterioles of the

TABLE I. Glomerular filtration rates and urine flow rates

GFR Urine Flow

ml *kg--’ * min-’

Control (mannitol only) 1.433 + 0.134 (15)

Mannitol control prior to salt load 1.287 -t 0.129 (14)

0.232 + 0.018 (15)

0.222 k 0.024 (14) RT nephrons branch at right angles from these intralob-

- . Following salt load, 35 meq/kg body wt 0.450 2 0.121 (4) 0.159 ? 0.030 (4) ular arteries. Previously pub1 (5) mannitol control 0.882 -+ 0.036 (97) 0.186 t 0.008 (101) Renal microvascular Datterns following 2.5% manni-

Values are means -+ SE. Figures in parentheses are number of clearance periods. tol infusion. The filling of the renal mi&ovasculature

1114 E. J. BRAUN

with Microfil was uniform and complete following the establishment of a diuresis caused by an intravenous infusion of 2.5% mannitol (Fig. 3). The even and complete filling of the renal vasculature would appear to indicate that the blood flow was uniform throughout the kidney during the mild mannitol diuresis. That the peripheral, superficial areas of kidney where the RT nephrons are located filled evenly indicates that the blood flow to these nephrons was not restricted during the infusion of 2.5% mannitol. Indeed, the intralobular arteries within the cortical lobules filled with Microfil (Fig. 4). The afferent arterioles and glomeruli of the RT nephrons can be plainly seen within the cortical lobules (Fig. 4).

Renal microvascular patterns following salt loading. The filling of the renal microvasculature with Microfil was incomplete following an intravenous salt load of 35 meq/kg (Fig. 3). The sparse filling of the vasculature was most pronounced in the peripheral areas of the kidneys where the RT nephrons are located (Fig. 5). The lack of filling indicates that blood flow to the superficial areas of the kidneys was restricted prior to the infusion of Microfil. The intralobular arteries within the cortical lobules filled but very few afferent arterioles and glomerular capillaries of RT nephrons filled with the Mi- crofil. Only about four capillary tufts can be seen in Fig. 5. The deeper areas of the kidneys at the bases of the medullary cones, where the glomeruli of the MT nephrons are located, fill more completely with Microfil following the intravenous salt load (Fig. 6).

DISCUSSION

The total-kidney GFR and urine flow measured during the present study were significantly higher than values previously measured for the desert quail. How- ever, in the present study, the GFR and urine flow for the mannitol controls and the controls prior to salt loading did not differ significantly. Thus, the effects of the mannitol infusion probably were the same for both groups of birds in the present study. Therefore, the changes seen in intrarenal blood flow distribution were not due to birds responding differently to the 2.5% man- nit01 infusion.

The group of birds that was salt loaded received 35 meq/kg body wt NaCl as salt load. In a previous study (6), the total-kidney GFR had decreased to 40% of control in desert quail that were salt loaded to a similar extent. When the single nephron glomerular filtration rates (SNGFRs) were evaluated at this point, no RT nephrons were found to be filtering. However, the MT nephrons continued to filter under these conditions at a rate of 12.8 nl/min (6). It was apparent that the blood flow to the RT nephrons was being regulated at some point in the vasculature leading to these nephrons.

The present study supports previous data which indicated that the number of filtering RT nephrons within the kidney of the desert quail varies depending on the state of hydration or salt balance of the bird. The Micro- fil infusions in the control studies (2.5% mannitol infusion only) produced casts of the renal m icrovasculature that clearly indicated flo w through the afferent arteri-

oles and into the glomerular capillaries of the RT nephrons. This would indicate that these nephrons were filtering during the 2.5% mannitol infusion. The Micro- fil passed through the glomerular capillaries, efferent arterioles, and into the peritubular capillary network surrounding the RT nephrons. Under conditions similar to these (2.5% mannitol infusion) the MT nephrons filtered at a rate of 14.6 nl/min and the RT nephrons at a rate of 6.4 nl/min with about 70% of the RT nephrons filtering (5).

As pointed out above, loaded, the RT nephrons

when desert stop filtering.

quail are It is clear

salt from

the Microfil casts- that there was a difference in the resistance to flow or tone of the renal vasculature of the birds that had received the salt load. The Microfil did not enter the vasculature in the peripheral regions of the kidney where the RT nephrons are located. The critical point where the Microfil perfusion of the renal vasculature stopped appeared to be at the level of the afferent arterioles of the RT nephrons. If the lack of filling of the vasculature can be taken to mean that there was no blood flow to the glomeruli of the RT nephrons, the results of the present study clearly sup- port the previous evidence which indicated that the RT nephrons stop filtering during periods of severe osmotic stress. The Microfil casts indicate that the RT nephrons stop filtering because of a vasconstriction at the level of the afferent arterioles leading to these nephrons. The intralobular arteries located within the cortical lobules filled with Microfil, indicating that these arteries were open at the time the Microfil was infused following salt loading.

During salt loading the MT nephrons continue to filter (6). This is also apparent from a study of the Microfil casts. The microvasculature was well filled with Microfil in the subcortical areas of the kidney where the MT nephrons are located (Fig. 6).

This regional blood flow within the avian kidney may be controlled by antidiuretic hormone. When arginine vasotocin (AVT), the natural antidiuretic hormone of birds was administered to desert quail which were re- ceiving an intravenous infusion of 2.5% mannitol, changes occurred in the SNGFRs of both the MT and RT nephrons and in the number of filtering RT nephrons (6). With low (2.25 and 4.25 vasopressor milliunits per kilogram), probably physiological doses of the hormone, the changes in the SNGFRs were small. However, there were significant reductions in the number of filtering RT nephrons (6). When large (45 vasopressor milliunits per kilogram), probably pharmacological doses of AVT were given, the RT nephrons stopped filtering entirely. This result resembled very much the results following artificial dehydration induced by salt loading. More- over, when the SNGFRs were measured in desert quail following the removal of the endogenous source of AVT by neurohypophysectomy, all the RT nephrons were found to be filtering (4). However, the SNGFRs of the RT nephrons after neurohypophysectomy were slightly lower than the SNGFRs measured for these nephrons under control conditions (4). Thus, it would appear that the intrarenal redistribution of blood flow in birds during periods of osmotic stress may be under the influence


afferent vein

reptilian type nephrons

central vein (efferent)

intralobular arteries

mammalian type nephron

FIG. 2. A diagrammatic representation of a portion of quail kid- (intralobular) enter each cortical lobule to supply glomeruli of RT

ney showing blood supply to MT and RT nephrons. Each cylindrical nephrons. These arteries form a symmetrical pattern about central cortical lobule has as its axis a central efferent vein. RT nephrons vein. Blood supply to MT nephrons is more random.

are arranged in a radiating pattern about central vein. Four arteries

FIG. 3. Kidneys from desert quail cleared in immersion oil to and completely filled with Microfil. Peripheral regions of vascula- display Microfil casts of renal vasculature. Kidney on left is from a ture within one on right did not fill with Microfil. Border of kidney bird that received only mannitol infusion. Kidney on right is from a on right can be seen as a faint outline. x 12. bird that was salt loaded. Vasculature within kidney on left is evenly

FIG. 4. A section of cleared kidney tissue from a bird that received vasculature in superficial regions of kidney where RT nephrons are

only mannitol infusion. Tissue was photographed at a higher magni- located. As can be seen, in some areas Microfil passed through fication than tissue in Fig. 3 to show even and complete filling of fine glomeruli into peritubular capillary network. x 50.

FIG. 5. A section of cleared kidney tissue from a bird that was salt superficial regions of kidney where RT nephrons are located. Few, if

loaded. Tissue was photographed at a higher magnification than any glomeruli or afferent arterioles can be seen filled with Microfil.

tissue in Fig. 3 to show incomplete filling of fine vasculature in x50.

1116


FIG. 6. A section of cleared kidney tissue from a bird that was salt loaded. Tissue is from deeper region of kidney where MT nephrons

of the antidiuretic hormone. Indeed, it has been sug- gested that the primary antidiuretic effect of AVT in the avian kidney may be a vascular action and not a tubular response (6).

While it is not certain that glomerular intermittency occurs within the kidneys of mammals (1, 7, 101, the results of the present study and previous work (5, 6, 8) with the desert quail clearly indicate that glomerular intermittency does occur in birds. The decrease in GFR that occurs because of the glomerular intermittency is one mechanism of conserving water during periods of stress. The reduction in GFR combined with a slow controlled increase in plasma osmolality, the excretion of ions in excess of water by the production of a more concentrated urine, and the excretion of ions with precipitated uric acid, all function as homeostatic mecha-

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nisms to conserve needed body water during periods of stress. These mechanisms may be more highly devel- oped in birds adapted to living in arid or semiarid regions. The desert quail, the bird used in these studies, is faced with limited supplies of water during much of the year in its natural habitat. Moreover, these birds have been reported to be able to survive without free water as long as succulent vegetation is available for consumption (11).

This study was supported by National Institutes of Health Re- search Grant Am-16294 and National Science Foundation Grant BMS75-10105.

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Intrarenal blood flow distribution in the desert quail - 2nd Chance