Pfiiigers Arch. 359, 127--135 (1975) 9 by Springer-Verlag 1975
Blood Flow in Mesenteric, Hepatic Portal and Renal Portal Veins of Chickens* P. D. Sturkie and A. Abati Department Environmental Physiology Cook College, Rutgers University Iqew Brunswick, New Jersey, U.S.A. Received March 24, 1975
~qummary. Blood flows were determined by electromagnetic probes placed upon the posterior vena cava (PVC), eoeeygeomesenterie vein (COCMV), mesenteric vein (MV), and hepatic portal vein (PV) of white Leghorn males. Blood flow in ml]min of non-fasted, unanesthetized males were as follows: per kg
MV
COCMV
PV
PVC
6.7
8.3
15.0
45.0
Withholding food for 24 hrs decreased flow significantly only in the MV and PVC. Anesthesia decreased flow in PVC, PV and COCMV. After ligation of PVC, blood was shunted from caudal areas and renal portal circulation r COCMV and liver. Ligation of PV caused a diversion of flow to renal portal eireulation and an increase in PVC flow and a reversal of direction of flow in COCMV.
Key words: Blood Flow in Renal Portal -- Hepatic Portal Circulations. Birds have a renal portal circulation b y which blood from the renal portal veins (afferent) is carried directly to the renal tubules. Sperber, (1960) demonstrated t h a t when a substance is injected into the femoral vein and into the renal portal vein, this substance is excreted b y the tubules on the injected side before it gets into the general circulation. Located a t the juncture of the renal vein and renal portal vein (see Fig. 1) is a prominent valve which apparently governs the flow of blood into the renal portal vein (Sturkie, 1965, 1970). Little is known eonerning the physiology of the valve, b u t it is presumed t h a t pressure and flow conditions in the renal portal veins, and renal veins m a y influence the opening and closing of the valve and thus the relative amounts of afferent venous blood supplying the kidney tubules. I t is known t h a t histamine and acetylcholine cause this valve to dose, and epinephrine causes it to open, based on in vitro studies (Renniek and Gandia, 1954). The renal portal system is connected to the hepatic portal system via of the eoceygeomesenteric vein, which serves as a shunt between * Supported in part by NSF grant BMS ~r 71-01593. Paper of the Journal Series New Jersey Agricultural Experiment Station.
128
P. D. Sturkie and A, Abati
these systems. I f the renal portal valve is closed, blood m a y be diverted through the coccygeomesenterie to the hepatic portal and to the liver. Under certain conditions, blood from the intestinal tract m a y be shunted to the kidney (Akester, 1967). This was based upon studies (Akester) involving the injection of a radiographic substance into the femoral vein whose passage was photographed at frequent intervals. Blood flow through the liver has been determined in the turkey by clearance techniques (Clarkson and Riehards, 1966) and in the chicken b y Sapirstein and H a r t m a n (1959) and Boelkins etal. (1973) who measured the distribution of radioactive substances. Liver flow in the turkey was 44.2 ml/kg and in the chicken 28.9 ml/min per bh'd. The latter figure represented 7.0 percent of the cardiac output and similar results were reported b y Sapirstein and Hartman. These values appear relatively lower than values reported for mammals whose values are highly variable depending on method of determination and other factors (Bradley, 1963; Grim, 1963). Blood flows of hepatic portal vein which represent 2/3 to 3/4 of liver flow likewise are highly variable and range from about 14 to 30 percent of the cardiac output, depending on the species and conditions (Grim, 1963). The object of this study was to determine the distribution of blood flow in the hepatic portal and renal portal circulations under varying conditions; specifically ~o measure flow in tha hepatic portal vein, eoecygeomesenterie vein and posterior vena eava before and after anesthesia, after fasting, and following changes in resistance to flow in the renal and hepatic circulations.
Materials and Methods White Leghorn male chickens, 4 to 6 months of age, and approaching sexual maturity, (average weight, 2.1 kg) were used in this investigation. The birds were restrained on a surgical board in a supine position. The wings were extended and tied or clamped into place, and the feet were tied to restrict movement. The bird was anesthetized via the brachial vein with a 30 mg/kg dose of sodium pentebarbital. The trachea was intubated and respiration was maintained artificially with a respiration pump (Harvard Apparatus Co., Inc.). ~eathers were removed from the area enclosed by the keel, the last rib on the right side and the upper part of the right leg. An abdominal incision of approximately 4--5 em in length was made roughly parallel to the last rib and ending near the upper part of the right leg. The body cavity was entered by blunt dissection and a 1--2 em section of the last two ribs was removed. The opening was enlarged with the use of a retractor. That portion of the posterior vena cava (PVC) which lies between the liver and the ~estes was carefully exposed (see Fig. 1). Next, a 1 cm segment of the coccygeomesenterie vein (COCMV) was isolated just below the point of entry of the mesenterie vein (MV). This section of the COCMV is sometimes referred to as the posterior mesenterie vein. A similar portion of the portal vein (PV) was isolated between the point of entry of the gastroduodenal vein (GDV) and the MV. In
Blood Flow in Mesenteric, Hepatic Portal and Renal Portal Circulations
129
Left jugular ~ l
~!
~:~
~ ''"
~
,
..,-
~
, Left pectoral
.
/e
Hepotic portal
-
',li AI) Ren~'
~
veMa CaVa
I
"" "". 9
'' LeftsuSdOvian
~Anterior
I~~. :--11" ~
Posterior yeN~ cova
~
---%%
ll} ;f.t
Internal . _ ~ ~ ~ i l l r
11 ,g__Cocr mesenteric
/ ~t-"-----Caudal hypogastric Right
Fig. 1. Venous system of birds. Main vessels shown in ventral view. Electromagnetic probes placed on vessels at points indicated by erossmarks. The hepatic portal vein (PV) is shown between gastroduodenal and mesenterie
some birds it was also possible to isolate a 1 cm segment of the MY just distal to the M~-COC1VW-PVjunction. Electromagnetic flow-meter probes (Carolina Medical Electronics, Inc.) were placed on the isolated segments of the PVC, COCMV, MV and PV, and were held in place by a system of clamps and supporting rods. Probe sizes varied according to vessel size. Typical probes used in this study had the following circumferences: PVC-10 mm and 12 mm probes; COCMV-8 mm and 9 mm probes; MV-7 mm and 8 mm probes; PV-8 mm and 9 mm probes. Simultaneous flow measurements of all isolatsd venous segments were possible once the probes were properly positioned. Under normal conditions, flow in the PV should equal the sum of MV and COCMV flow (see figure) thus providing a cheek on probe placement. Blood flows were recorded over a 30 see period and the results averaged. Isolated venous segments of various sizes (eg. PVC, PV and jugular vein) were used to calibrate probes of different circumferences. Chicken blood was infused through the vessels at variable flow rates (1.15 ml/min to 114.6 ml/min), and the response of the probes was linear throughout this flow range. 9 PfltigersArch., Vol.359
130
P. D, Sturkie and A. Abati
Two groups of birds were used in this study. One group was fasted for 24 hrs while the other group was non-fasted. After surgery and Probe placement, the birds were allowed to recover from the general anesthesia, and a local anesthetic (2~ Procaine-HC1) was applied to the wound area. Ligation experiments were carried out by pinching off one of the four venous segments and recording simultaneous changes in the other three segments. After data were obtained from unanesthetized birds, they were reanesthetized (30 mg/kg sodium pentobarbital) and the effect of anesthesia on blood flow in these veins was recorded for 50 rain. Ligation experiments were Mso carried out on fully anesthetized birds.
Results A c o m p a r i s o n o f m e a n b lo o d flows in t h e MV, COCMV, P V , a n d P V C o f f a s t e d a n d n o n f a s t e d , a n e s t h e t i z e d a n d n o n a n e s t h e t i z e d birds is sh o wn in T a b l e 1. All d a t a on a n e s t h e t i z e d birds r e p r e s e n t flow v a l u e s o b t a i n e d a n d a v e r a g e d d u r i n g a 1 5 - - 5 0 m i n p e r i o d following i n j e c t i o n o f a single i n t r a v e n o u s dose o f n e m b u t a l (30 mg/kg).
EHect o] Fasting on Blood Flow M e a n b l o o d flows were s o m e w h a t g r e a t e r in t h e n o n f a s t e d birds in b o t h a n e s t h e t i z e d a n d n o n a n e s t h e t i z e d groups, w i t h t h e e x c e p t i o n o f
Table 1. Blood flow (ml/min) in mesenteric (MV) and coccygeomesenterie (COCMV) vein, portal vein (PV) and posterior vena eava (PVC) in birds fed and fasted, and anesthetized and non-anesthetized Blood flow ml/m
Nonanesthetized MV
Anesthetized a
COC1VfVPV
PVC
MV
C O C M VPV
PVC
9.67 1.44 18 4.83
13.61d 1.46 18 6.87
23.22 a 1.77 18 11.68
55.61e 4.17 18 27.98
13.80b 1.18 10 6.34
12.67a 2.18 18 5.86
26.50 a 3.12 18 12.13
69.28 b,c 4.64 18 31.94
Fasted Per bird 2 SE I~ Per kg
9.55 .97 22 4.74
19.32 2.57 22 9.47
28.86 3.06 22 14.21
80.14 4.22 22 39.72 l~on-fasted
Per bird .~ SE N Per kg a b e a
14.67b 1.39 15 6.82
18.13 2.15 23 8.16
32.78 2.55 23 14.80
98.35 b 6.51 23 45.30
Average of values from 15 to 50 min. after injection of nembutal. Difference from fasted significant at P ~ 0.01. Difference from nonanesthetized significant at P < 0.01). Difference from nonanesthetized significant at P ~ 0.05) T ValNzs.
Blood Flow in Mesenteric,Hepatic Portal and Renal Portal Circulations
131
COCMV blood flows which were not significantly different. Differences between blood flows of fasted and nonfasted birds were statistically significant (P < 0.01) in only the PVC and the MV. Mean PVC blood flows from nonanestheized and anesthetized birds were 18.51~ and 19.73~ greater, respectively, in the nonfasted group than they were in the fasted group. MV blood flows from nonanesthetized and anesthetized birds averaged 34.90~ and 29.930/0 greater, respectively, in the nonfasted group than in the fasted group. State o/Anesthesia on ~Blood Flow
The effect of a single intravenous dose of nembutal (30 mg/kg) on PVC, COCMV, MV, and PV blood flow in fasted birds is shown in Fig. 2. Blood flow in these vessels decreased gradually during the 50 rain period following injection. Similar results were obtained from nonfasted birds. PVC blood flows had decreased 35.39~ in fasted and 37.38~ in nonfasted birds by the end of the 50 rain observation period. PV flows decreased 36.900/o in fasted birds and 31.45 ~ in nonfasted birds, while COCMV flows decreased 41.92~ and 40.370/0 in fasted and nonfasted birds, respectively. At the end of 50 rain, M-V flows had not decreased significantly in either group. During the first 10 min following injection
I00 9O
80 ,-- 70 60
PVC
"E
so
i
40 30" 20:
PV cocMv
I0.~ I
|
5
I0
I
I
15 20
Time (in minutes)-after
I
25
I
30
J
35
I
40
I
i
45
50
MV
injection of nembutal (30 mcj/Kg)
Fig.2. Blood flow in posterior vena eava (PVC), hepatic portal vein (PV), coeeegeomesenteric vein (COCM~) and mesenteric vein (MV), of white Leghorn cockerels (Fasted) 9*
132
P. D. Sturkie and A. Abati
of nembutal, PV flows increased slightly, but not significantly, in both fasted and nonfasted birds. The initial increase in PV flow, as shown in Fig. 2, is associated with a slight increase in MV flow during this same time period. I f blood flows, which were recorded for the PVC, COCMV, and PV are averaged during the 15 to 50 rain period following nembutal injection, (deep anesthesia) they are found to be significantly lower than during the unanesthetized state in both fasted and nonfasted birds. These data are summarized in Table 1. PVC blood flows were 30.61~ lower in fasted anesthetized birds and 29.56~ lower in nonfasted anesthetized birds. Mean PV flows were 19.54~ and 19.16~ lower in fasted and nonfasted anesthetized birds, respectively. Similar differences were observed with COCMV mean blood flows where fasted birds were 29.55~ lower and nonfasted birds 30.12~ lower during anesthesia. Mean MV blood flow did not differ significantly during anesthesia in either fasted or nonfasted birds.
EHects o/Anesthesia on Blood Pressure Sodium pentobarbital anesthesia decreases arterial blood pressure significantly, and the drop is greatest (50--60 mm Hg systolic) within 2--50 rain after administration. I t then rises slowly during the next 30 min, but it still is 30--40 mm Hg below normal at the end of this time. The initial level of systolic blood pressures ranged from 140-- 165 mm Hg. Blood flow in PVC continued to fall following anesthesia (Fig.2), whereas the changes in flows in PV, COCMV, and CMV were not as great nor as consistent. In fact, there was an initial increase in flow in these veins during the initial drop in blood pressure (5--10 min) and then a slight but continued decrease in flow during the remainder of the period.
EHect o/Ligation on Blood _Flow The effects of ligation on blood flow in the MV, COCMV, PV and PVC of fasted birds are shown in Table 2. Only data on fasted birds are shown here since the latter are the most extensive, and since results of the same magnitude were obtained from fasted and nonfasted birds. Anesthesia had no effect on the response of the vessels to ligation. Thus, data in Table 2 reflect the average of both anesthetized and nonanesthetized birds. Ligation of the PVC resulted in a significant increase in both COCMV and PV blood flow, and a slight but insignificant decrease in MV blood flow. Sample data from Table 2 show that the increase in fasted PV blood flow (24.08 ml/min) was 1.70 ml/min less than the COCMV blood
Blood Flow in Mesenteric, Hepatic Portal and Renal Portal Circulations
133
Table 2. The effects ofligation of certain veins (one at a time) on blood flow (ml/min) in mesenteric (MV), eoccygeomesenteric (COCMV), portal vein (PV) and posterior vena cava (PVC) of 27 white Leghorn male chickens (fasted) Blood flow before (B) and during (D) ligation Vein ligated
MV B
PVC
J~ SE
D
COCMV
PV
B
B
D
PVC D
B
D ---
9.44 7.67 1.00 0.95 1.77
15.81 41.59 2.00 3.06 25.78
25.44 49.52 2.15 3.17 24.08
--* --
15.81 --7.11 a 2.00 0.87 --
---
Diff.b
9.44 7.04 1.00 0.85 2.33
66.19 89.15 3.63 4.83 22..96
COCMV ~ SE Diff.b
9.22 11.19 1.05 1.00 1.43
---
25.44 11.22 2.15 1.00 14.22
66.19 82.11 3.63 5.05 15.92
MV
---
15.81 1 7 . 3 0 2.00 1.99 1.49
25.44 17.30 2.15 1.99 8.14
65.15 63.67 3.48 3.47 1.48
Diff.b PV
Diff.b
X SE
~ SE --
----
----
----
--
a Minus sign indicates blood flow in reverse direction, away from the liver, toward the PVC. -- * Blank = 0 = zero = no blow measured b Difference in flow between pre and post ligation < 3 not significant.
flow increase (25.78 ml/min). This m a y be e x p l a i n e d b y the fact t h a t MV blood flow decreased 1.77 m l / m i n d u r i n g PVC ligation, a n d P V flow m u s t e q u a l the s u m of MV flow a n d COCMV flow i n this system. W h e n the P V was clamped, blood flow i n the COCMV reversed direction a n d flowed a w a y from the liver t o w a r d the PVC. The m a g n i t u d e of the COCMV blood flow d u r i n g P V l i g a t i o n was d e t e r m i n e d b y blood flow from the MV. Sample d a t a from T a b l e 2 illustrates this p o i n t clearly. W h e n the P V ' s from fasted birds were clamped, m e a n MV blood flow decreased slightly to 7.04 ~: 0.85 m l / m i n , while COCMV flow decreased significantly from 1 5 . 8 1 - ~ 2.00 m l ] m i n to 7.11 :i: 0.87 m l / m i n i n the opposite direction (indicated b y a m i n u s sign i n T a b l e 2). D u r i n g this t i m e the PVC flow increased b y 22.96 m l / m i n , a n a m o u n t a p p r o x i m a t e l y e q u a l to the s u m of the original COCMV blood flow a n d the p o s t l i g a t i o n CMV blood flow (15.81 m l / m i n + 7.04 m l / m i n = 22.85 ml/min). Ligat i o n of COCMV resulted i n a slight increase (insignificant) i n MV blood flow a n d a decrease i n P V blood flow to a value a p p r o x i m a t e l y e q u a l
134
P. D. Sturkie and A. Abati
to the post-ligation MV blood flow. PVC blood flow increased during COCMV ]igation b y an amount approximately equal to that of the preligation COCMV blood flow (Table 2). Following ligation of the MV, mean COCMV blood flow increased slightly, while mean PV blood flow decreased to a value equal to the new COCMV blood flow.
Discussion Fasting decreased blood flow in most of the veins studied and this was as expected, but flow in the shunt vessel (COCMV) was not appreciably changed. The reason for this is not evident, but it m a y suggest t h a t some blood from legs, kidney, and caudal areas of body may be shunted through COCMV in an attempt to maintain normal hepatic portal flow (PV) which was decreased relatively less than mesenteric vein flow (MV). This possibility remains, however, to be tested. Moreover, the level of blood flow in the COCMV under all conditions was consistently higher than in the MV, and this was unexpected. Actually the MV drains a larger area (all of the small intestine other than duodenum) than the COCM, which drains the smaller area of large intestine, but it may also receive shunted blood from other areas including veins of legs and renal portals. Differences in pressures in COCMV and MV, if such exist, could account for differences in flow, but this remains to be determined. There was a fairly consistent drop in blood flow in the posterior vena cava (PV) following anesthesia and there was also a drop in central blood pressure particularly during the initial stages of anesthesia (first 10 min) and this m a y have accounted for some of the decrease as might be expected. During the same period, however, there was no drop in flow in PV, CM, and COCMV, but a slight increase. This might suggest that blood from the caudal areas including the legs and kidney was shunted through these veins to the liver. This shunting may have been caused in part by the partial closure of the renal portal valves, resulting from anesthesia and the release of acetylch01ine which has been reported to close the valve in vitro (Renniek and Gandia, 1954). The effect of these agents on the valve in vivo remains to be determined. The shunting of blood flow to the liver or kidney was demonstrated b y ligation of the appropriate blood vessels, but the extent and direction of the shunting under normal conditions is not known, although previous workers (Akester, 1967 ; Clarkson and Richards, 1965) had reported t h a t blood flow could be toward kidney or liver. The results of this study indicate that flow was in nearly all instances directed toward the liver.
Blood Flow in Mesenteric, Hepatic Portal and Renal Portal Circulations
135
This m a y h a v e been influenced b y t h e f a c t t h a t t h e a n i m a l s were r e s t r a i n ed in a supine p o s i t i o n . The e x t e n t to which p o s i t i o n o f t h e b o d y a n d g r a v i t y influence d i r e c t i o n o f flow is n o t known.
References Akester, A . R . : Renal portal shunts in the kidney of domestic fowl. J. Anat. (Lend.) 191, 569--594 (1967) Boolkins, N. N., Mueller, W. g., Hall, K. L.: Cardiac output distribution in the laying hen during shell formation. Comp. Biochem. Physiol. 46A, 735--743 (1973) Bradley, S. E. : The hepatic circulation Handbook of Physiology. W . F . Hamilton and P. Dew Eds. Circulation, Vol. II, pp. 1387--1438 (1963) Clarkson, M. J., Richards, T. G.: Liver blood flow in the turkey in physiology of the domestic fowl. Chapter 33, pp. 294--301. C. Herren-Smith and E.C. Amoroso, Eds. Edinburgh: Oliver & Boyd 1965 Grim, E.: The flow of blood in the mesenteric vessels. Handbook of Physiology. W. F. Hamilton and P. Dew Eds. Circulation, Vol. II, pp. 1439--1456 (1963) Rennick, B. R., Gandia, H.: Pharmacology of the smooth muscle valve in renal portal circulation of birds. Prec. See. exp. Biol. (N.Y.) 85, 234--236 (1954) Sapirstein, L. A., Hartman, F . A . : Cardiac output and its distribution in the chicken. Amer. J. Physiol. 196, 751--752 (1959) Sperber, L: Exretion, Chap. 12, Vol. I: Biology and Comparative Physiology of Birds, A. J. Marshall, Ed., pp. 469--492. New York: Academic Press 1960 Sturkie, P. D. : Kidneys and Urine, Chapter 13: Avian Physiology, 2nd edit. Ithaca, New York: Cornell Press 1965 Sturkie, P. D. : Circulation in Ayes. Fed. Prec. 99, 1674--1679 (1970) P. D. Sturkie A. Abati Department of Environmental Physiology Cook College Rutgers University New Brunswick, New Jersey 08903, U.S.A.
Blood Flow in Mesenteric, Hepatic Portal and Renal Portal Veins of Chickens* P. D. Sturkie and A. Abati Department Environmental Physiology Cook College, Rutgers University Iqew Brunswick, New Jersey, U.S.A. Received March 24, 1975
~qummary. Blood flows were determined by electromagnetic probes placed upon the posterior vena cava (PVC), eoeeygeomesenterie vein (COCMV), mesenteric vein (MV), and hepatic portal vein (PV) of white Leghorn males. Blood flow in ml]min of non-fasted, unanesthetized males were as follows: per kg
MV
COCMV
PV
PVC
6.7
8.3
15.0
45.0
Withholding food for 24 hrs decreased flow significantly only in the MV and PVC. Anesthesia decreased flow in PVC, PV and COCMV. After ligation of PVC, blood was shunted from caudal areas and renal portal circulation r COCMV and liver. Ligation of PV caused a diversion of flow to renal portal eireulation and an increase in PVC flow and a reversal of direction of flow in COCMV.
Key words: Blood Flow in Renal Portal -- Hepatic Portal Circulations. Birds have a renal portal circulation b y which blood from the renal portal veins (afferent) is carried directly to the renal tubules. Sperber, (1960) demonstrated t h a t when a substance is injected into the femoral vein and into the renal portal vein, this substance is excreted b y the tubules on the injected side before it gets into the general circulation. Located a t the juncture of the renal vein and renal portal vein (see Fig. 1) is a prominent valve which apparently governs the flow of blood into the renal portal vein (Sturkie, 1965, 1970). Little is known eonerning the physiology of the valve, b u t it is presumed t h a t pressure and flow conditions in the renal portal veins, and renal veins m a y influence the opening and closing of the valve and thus the relative amounts of afferent venous blood supplying the kidney tubules. I t is known t h a t histamine and acetylcholine cause this valve to dose, and epinephrine causes it to open, based on in vitro studies (Renniek and Gandia, 1954). The renal portal system is connected to the hepatic portal system via of the eoceygeomesenteric vein, which serves as a shunt between * Supported in part by NSF grant BMS ~r 71-01593. Paper of the Journal Series New Jersey Agricultural Experiment Station.
128
P. D. Sturkie and A, Abati
these systems. I f the renal portal valve is closed, blood m a y be diverted through the coccygeomesenterie to the hepatic portal and to the liver. Under certain conditions, blood from the intestinal tract m a y be shunted to the kidney (Akester, 1967). This was based upon studies (Akester) involving the injection of a radiographic substance into the femoral vein whose passage was photographed at frequent intervals. Blood flow through the liver has been determined in the turkey by clearance techniques (Clarkson and Riehards, 1966) and in the chicken b y Sapirstein and H a r t m a n (1959) and Boelkins etal. (1973) who measured the distribution of radioactive substances. Liver flow in the turkey was 44.2 ml/kg and in the chicken 28.9 ml/min per bh'd. The latter figure represented 7.0 percent of the cardiac output and similar results were reported b y Sapirstein and Hartman. These values appear relatively lower than values reported for mammals whose values are highly variable depending on method of determination and other factors (Bradley, 1963; Grim, 1963). Blood flows of hepatic portal vein which represent 2/3 to 3/4 of liver flow likewise are highly variable and range from about 14 to 30 percent of the cardiac output, depending on the species and conditions (Grim, 1963). The object of this study was to determine the distribution of blood flow in the hepatic portal and renal portal circulations under varying conditions; specifically ~o measure flow in tha hepatic portal vein, eoecygeomesenterie vein and posterior vena eava before and after anesthesia, after fasting, and following changes in resistance to flow in the renal and hepatic circulations.
Materials and Methods White Leghorn male chickens, 4 to 6 months of age, and approaching sexual maturity, (average weight, 2.1 kg) were used in this investigation. The birds were restrained on a surgical board in a supine position. The wings were extended and tied or clamped into place, and the feet were tied to restrict movement. The bird was anesthetized via the brachial vein with a 30 mg/kg dose of sodium pentebarbital. The trachea was intubated and respiration was maintained artificially with a respiration pump (Harvard Apparatus Co., Inc.). ~eathers were removed from the area enclosed by the keel, the last rib on the right side and the upper part of the right leg. An abdominal incision of approximately 4--5 em in length was made roughly parallel to the last rib and ending near the upper part of the right leg. The body cavity was entered by blunt dissection and a 1--2 em section of the last two ribs was removed. The opening was enlarged with the use of a retractor. That portion of the posterior vena cava (PVC) which lies between the liver and the ~estes was carefully exposed (see Fig. 1). Next, a 1 cm segment of the coccygeomesenterie vein (COCMV) was isolated just below the point of entry of the mesenterie vein (MV). This section of the COCMV is sometimes referred to as the posterior mesenterie vein. A similar portion of the portal vein (PV) was isolated between the point of entry of the gastroduodenal vein (GDV) and the MV. In
Blood Flow in Mesenteric, Hepatic Portal and Renal Portal Circulations
129
Left jugular ~ l
~!
~:~
~ ''"
~
,
..,-
~
, Left pectoral
.
/e
Hepotic portal
-
',li AI) Ren~'
~
veMa CaVa
I
"" "". 9
'' LeftsuSdOvian
~Anterior
I~~. :--11" ~
Posterior yeN~ cova
~
---%%
ll} ;f.t
Internal . _ ~ ~ ~ i l l r
11 ,g__Cocr mesenteric
/ ~t-"-----Caudal hypogastric Right
Fig. 1. Venous system of birds. Main vessels shown in ventral view. Electromagnetic probes placed on vessels at points indicated by erossmarks. The hepatic portal vein (PV) is shown between gastroduodenal and mesenterie
some birds it was also possible to isolate a 1 cm segment of the MY just distal to the M~-COC1VW-PVjunction. Electromagnetic flow-meter probes (Carolina Medical Electronics, Inc.) were placed on the isolated segments of the PVC, COCMV, MV and PV, and were held in place by a system of clamps and supporting rods. Probe sizes varied according to vessel size. Typical probes used in this study had the following circumferences: PVC-10 mm and 12 mm probes; COCMV-8 mm and 9 mm probes; MV-7 mm and 8 mm probes; PV-8 mm and 9 mm probes. Simultaneous flow measurements of all isolatsd venous segments were possible once the probes were properly positioned. Under normal conditions, flow in the PV should equal the sum of MV and COCMV flow (see figure) thus providing a cheek on probe placement. Blood flows were recorded over a 30 see period and the results averaged. Isolated venous segments of various sizes (eg. PVC, PV and jugular vein) were used to calibrate probes of different circumferences. Chicken blood was infused through the vessels at variable flow rates (1.15 ml/min to 114.6 ml/min), and the response of the probes was linear throughout this flow range. 9 PfltigersArch., Vol.359
130
P. D, Sturkie and A. Abati
Two groups of birds were used in this study. One group was fasted for 24 hrs while the other group was non-fasted. After surgery and Probe placement, the birds were allowed to recover from the general anesthesia, and a local anesthetic (2~ Procaine-HC1) was applied to the wound area. Ligation experiments were carried out by pinching off one of the four venous segments and recording simultaneous changes in the other three segments. After data were obtained from unanesthetized birds, they were reanesthetized (30 mg/kg sodium pentobarbital) and the effect of anesthesia on blood flow in these veins was recorded for 50 rain. Ligation experiments were Mso carried out on fully anesthetized birds.
Results A c o m p a r i s o n o f m e a n b lo o d flows in t h e MV, COCMV, P V , a n d P V C o f f a s t e d a n d n o n f a s t e d , a n e s t h e t i z e d a n d n o n a n e s t h e t i z e d birds is sh o wn in T a b l e 1. All d a t a on a n e s t h e t i z e d birds r e p r e s e n t flow v a l u e s o b t a i n e d a n d a v e r a g e d d u r i n g a 1 5 - - 5 0 m i n p e r i o d following i n j e c t i o n o f a single i n t r a v e n o u s dose o f n e m b u t a l (30 mg/kg).
EHect o] Fasting on Blood Flow M e a n b l o o d flows were s o m e w h a t g r e a t e r in t h e n o n f a s t e d birds in b o t h a n e s t h e t i z e d a n d n o n a n e s t h e t i z e d groups, w i t h t h e e x c e p t i o n o f
Table 1. Blood flow (ml/min) in mesenteric (MV) and coccygeomesenterie (COCMV) vein, portal vein (PV) and posterior vena eava (PVC) in birds fed and fasted, and anesthetized and non-anesthetized Blood flow ml/m
Nonanesthetized MV
Anesthetized a
COC1VfVPV
PVC
MV
C O C M VPV
PVC
9.67 1.44 18 4.83
13.61d 1.46 18 6.87
23.22 a 1.77 18 11.68
55.61e 4.17 18 27.98
13.80b 1.18 10 6.34
12.67a 2.18 18 5.86
26.50 a 3.12 18 12.13
69.28 b,c 4.64 18 31.94
Fasted Per bird 2 SE I~ Per kg
9.55 .97 22 4.74
19.32 2.57 22 9.47
28.86 3.06 22 14.21
80.14 4.22 22 39.72 l~on-fasted
Per bird .~ SE N Per kg a b e a
14.67b 1.39 15 6.82
18.13 2.15 23 8.16
32.78 2.55 23 14.80
98.35 b 6.51 23 45.30
Average of values from 15 to 50 min. after injection of nembutal. Difference from fasted significant at P ~ 0.01. Difference from nonanesthetized significant at P < 0.01). Difference from nonanesthetized significant at P ~ 0.05) T ValNzs.
Blood Flow in Mesenteric,Hepatic Portal and Renal Portal Circulations
131
COCMV blood flows which were not significantly different. Differences between blood flows of fasted and nonfasted birds were statistically significant (P < 0.01) in only the PVC and the MV. Mean PVC blood flows from nonanestheized and anesthetized birds were 18.51~ and 19.73~ greater, respectively, in the nonfasted group than they were in the fasted group. MV blood flows from nonanesthetized and anesthetized birds averaged 34.90~ and 29.930/0 greater, respectively, in the nonfasted group than in the fasted group. State o/Anesthesia on ~Blood Flow
The effect of a single intravenous dose of nembutal (30 mg/kg) on PVC, COCMV, MV, and PV blood flow in fasted birds is shown in Fig. 2. Blood flow in these vessels decreased gradually during the 50 rain period following injection. Similar results were obtained from nonfasted birds. PVC blood flows had decreased 35.39~ in fasted and 37.38~ in nonfasted birds by the end of the 50 rain observation period. PV flows decreased 36.900/o in fasted birds and 31.45 ~ in nonfasted birds, while COCMV flows decreased 41.92~ and 40.370/0 in fasted and nonfasted birds, respectively. At the end of 50 rain, M-V flows had not decreased significantly in either group. During the first 10 min following injection
I00 9O
80 ,-- 70 60
PVC
"E
so
i
40 30" 20:
PV cocMv
I0.~ I
|
5
I0
I
I
15 20
Time (in minutes)-after
I
25
I
30
J
35
I
40
I
i
45
50
MV
injection of nembutal (30 mcj/Kg)
Fig.2. Blood flow in posterior vena eava (PVC), hepatic portal vein (PV), coeeegeomesenteric vein (COCM~) and mesenteric vein (MV), of white Leghorn cockerels (Fasted) 9*
132
P. D. Sturkie and A. Abati
of nembutal, PV flows increased slightly, but not significantly, in both fasted and nonfasted birds. The initial increase in PV flow, as shown in Fig. 2, is associated with a slight increase in MV flow during this same time period. I f blood flows, which were recorded for the PVC, COCMV, and PV are averaged during the 15 to 50 rain period following nembutal injection, (deep anesthesia) they are found to be significantly lower than during the unanesthetized state in both fasted and nonfasted birds. These data are summarized in Table 1. PVC blood flows were 30.61~ lower in fasted anesthetized birds and 29.56~ lower in nonfasted anesthetized birds. Mean PV flows were 19.54~ and 19.16~ lower in fasted and nonfasted anesthetized birds, respectively. Similar differences were observed with COCMV mean blood flows where fasted birds were 29.55~ lower and nonfasted birds 30.12~ lower during anesthesia. Mean MV blood flow did not differ significantly during anesthesia in either fasted or nonfasted birds.
EHects o/Anesthesia on Blood Pressure Sodium pentobarbital anesthesia decreases arterial blood pressure significantly, and the drop is greatest (50--60 mm Hg systolic) within 2--50 rain after administration. I t then rises slowly during the next 30 min, but it still is 30--40 mm Hg below normal at the end of this time. The initial level of systolic blood pressures ranged from 140-- 165 mm Hg. Blood flow in PVC continued to fall following anesthesia (Fig.2), whereas the changes in flows in PV, COCMV, and CMV were not as great nor as consistent. In fact, there was an initial increase in flow in these veins during the initial drop in blood pressure (5--10 min) and then a slight but continued decrease in flow during the remainder of the period.
EHect o/Ligation on Blood _Flow The effects of ligation on blood flow in the MV, COCMV, PV and PVC of fasted birds are shown in Table 2. Only data on fasted birds are shown here since the latter are the most extensive, and since results of the same magnitude were obtained from fasted and nonfasted birds. Anesthesia had no effect on the response of the vessels to ligation. Thus, data in Table 2 reflect the average of both anesthetized and nonanesthetized birds. Ligation of the PVC resulted in a significant increase in both COCMV and PV blood flow, and a slight but insignificant decrease in MV blood flow. Sample data from Table 2 show that the increase in fasted PV blood flow (24.08 ml/min) was 1.70 ml/min less than the COCMV blood
Blood Flow in Mesenteric, Hepatic Portal and Renal Portal Circulations
133
Table 2. The effects ofligation of certain veins (one at a time) on blood flow (ml/min) in mesenteric (MV), eoccygeomesenteric (COCMV), portal vein (PV) and posterior vena cava (PVC) of 27 white Leghorn male chickens (fasted) Blood flow before (B) and during (D) ligation Vein ligated
MV B
PVC
J~ SE
D
COCMV
PV
B
B
D
PVC D
B
D ---
9.44 7.67 1.00 0.95 1.77
15.81 41.59 2.00 3.06 25.78
25.44 49.52 2.15 3.17 24.08
--* --
15.81 --7.11 a 2.00 0.87 --
---
Diff.b
9.44 7.04 1.00 0.85 2.33
66.19 89.15 3.63 4.83 22..96
COCMV ~ SE Diff.b
9.22 11.19 1.05 1.00 1.43
---
25.44 11.22 2.15 1.00 14.22
66.19 82.11 3.63 5.05 15.92
MV
---
15.81 1 7 . 3 0 2.00 1.99 1.49
25.44 17.30 2.15 1.99 8.14
65.15 63.67 3.48 3.47 1.48
Diff.b PV
Diff.b
X SE
~ SE --
----
----
----
--
a Minus sign indicates blood flow in reverse direction, away from the liver, toward the PVC. -- * Blank = 0 = zero = no blow measured b Difference in flow between pre and post ligation < 3 not significant.
flow increase (25.78 ml/min). This m a y be e x p l a i n e d b y the fact t h a t MV blood flow decreased 1.77 m l / m i n d u r i n g PVC ligation, a n d P V flow m u s t e q u a l the s u m of MV flow a n d COCMV flow i n this system. W h e n the P V was clamped, blood flow i n the COCMV reversed direction a n d flowed a w a y from the liver t o w a r d the PVC. The m a g n i t u d e of the COCMV blood flow d u r i n g P V l i g a t i o n was d e t e r m i n e d b y blood flow from the MV. Sample d a t a from T a b l e 2 illustrates this p o i n t clearly. W h e n the P V ' s from fasted birds were clamped, m e a n MV blood flow decreased slightly to 7.04 ~: 0.85 m l / m i n , while COCMV flow decreased significantly from 1 5 . 8 1 - ~ 2.00 m l ] m i n to 7.11 :i: 0.87 m l / m i n i n the opposite direction (indicated b y a m i n u s sign i n T a b l e 2). D u r i n g this t i m e the PVC flow increased b y 22.96 m l / m i n , a n a m o u n t a p p r o x i m a t e l y e q u a l to the s u m of the original COCMV blood flow a n d the p o s t l i g a t i o n CMV blood flow (15.81 m l / m i n + 7.04 m l / m i n = 22.85 ml/min). Ligat i o n of COCMV resulted i n a slight increase (insignificant) i n MV blood flow a n d a decrease i n P V blood flow to a value a p p r o x i m a t e l y e q u a l
134
P. D. Sturkie and A. Abati
to the post-ligation MV blood flow. PVC blood flow increased during COCMV ]igation b y an amount approximately equal to that of the preligation COCMV blood flow (Table 2). Following ligation of the MV, mean COCMV blood flow increased slightly, while mean PV blood flow decreased to a value equal to the new COCMV blood flow.
Discussion Fasting decreased blood flow in most of the veins studied and this was as expected, but flow in the shunt vessel (COCMV) was not appreciably changed. The reason for this is not evident, but it m a y suggest t h a t some blood from legs, kidney, and caudal areas of body may be shunted through COCMV in an attempt to maintain normal hepatic portal flow (PV) which was decreased relatively less than mesenteric vein flow (MV). This possibility remains, however, to be tested. Moreover, the level of blood flow in the COCMV under all conditions was consistently higher than in the MV, and this was unexpected. Actually the MV drains a larger area (all of the small intestine other than duodenum) than the COCM, which drains the smaller area of large intestine, but it may also receive shunted blood from other areas including veins of legs and renal portals. Differences in pressures in COCMV and MV, if such exist, could account for differences in flow, but this remains to be determined. There was a fairly consistent drop in blood flow in the posterior vena cava (PV) following anesthesia and there was also a drop in central blood pressure particularly during the initial stages of anesthesia (first 10 min) and this m a y have accounted for some of the decrease as might be expected. During the same period, however, there was no drop in flow in PV, CM, and COCMV, but a slight increase. This might suggest that blood from the caudal areas including the legs and kidney was shunted through these veins to the liver. This shunting may have been caused in part by the partial closure of the renal portal valves, resulting from anesthesia and the release of acetylch01ine which has been reported to close the valve in vitro (Renniek and Gandia, 1954). The effect of these agents on the valve in vivo remains to be determined. The shunting of blood flow to the liver or kidney was demonstrated b y ligation of the appropriate blood vessels, but the extent and direction of the shunting under normal conditions is not known, although previous workers (Akester, 1967 ; Clarkson and Richards, 1965) had reported t h a t blood flow could be toward kidney or liver. The results of this study indicate that flow was in nearly all instances directed toward the liver.
Blood Flow in Mesenteric, Hepatic Portal and Renal Portal Circulations
135
This m a y h a v e been influenced b y t h e f a c t t h a t t h e a n i m a l s were r e s t r a i n ed in a supine p o s i t i o n . The e x t e n t to which p o s i t i o n o f t h e b o d y a n d g r a v i t y influence d i r e c t i o n o f flow is n o t known.
References Akester, A . R . : Renal portal shunts in the kidney of domestic fowl. J. Anat. (Lend.) 191, 569--594 (1967) Boolkins, N. N., Mueller, W. g., Hall, K. L.: Cardiac output distribution in the laying hen during shell formation. Comp. Biochem. Physiol. 46A, 735--743 (1973) Bradley, S. E. : The hepatic circulation Handbook of Physiology. W . F . Hamilton and P. Dew Eds. Circulation, Vol. II, pp. 1387--1438 (1963) Clarkson, M. J., Richards, T. G.: Liver blood flow in the turkey in physiology of the domestic fowl. Chapter 33, pp. 294--301. C. Herren-Smith and E.C. Amoroso, Eds. Edinburgh: Oliver & Boyd 1965 Grim, E.: The flow of blood in the mesenteric vessels. Handbook of Physiology. W. F. Hamilton and P. Dew Eds. Circulation, Vol. II, pp. 1439--1456 (1963) Rennick, B. R., Gandia, H.: Pharmacology of the smooth muscle valve in renal portal circulation of birds. Prec. See. exp. Biol. (N.Y.) 85, 234--236 (1954) Sapirstein, L. A., Hartman, F . A . : Cardiac output and its distribution in the chicken. Amer. J. Physiol. 196, 751--752 (1959) Sperber, L: Exretion, Chap. 12, Vol. I: Biology and Comparative Physiology of Birds, A. J. Marshall, Ed., pp. 469--492. New York: Academic Press 1960 Sturkie, P. D. : Kidneys and Urine, Chapter 13: Avian Physiology, 2nd edit. Ithaca, New York: Cornell Press 1965 Sturkie, P. D. : Circulation in Ayes. Fed. Prec. 99, 1674--1679 (1970) P. D. Sturkie A. Abati Department of Environmental Physiology Cook College Rutgers University New Brunswick, New Jersey 08903, U.S.A.
