389
Dietary Sodium Chloride Increases Blood
Pressure in Obese Zucker Rats
Sreenivas R. Reddy and Theodore A. Kotchen
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In the rat, elevated arterial pressure is not consistently associated with obesity. The purpose of this study
was to compare measurements of blood pressure, cardiac output, and total peripheral resistance in obese
and lean Zucker rats on different NaCI intakes. Obese and lean rats drank either water or isotonic NaCl
for 18 days. Tail systolic blood pressures of saline-drinking obese rats were higher than all other groups
(p<0.05). NaCl intake did not affect blood pressure in lean rats, and blood pressures of water-drinking
obese rats did not differ from those of lean controls. In a subsequent experiment, direct arterial pressures
and cardiac outputs (thermodilution) were measured in separate groups of conscious rats that had been
maintained on a 1% or 4% NaCl intake for 12 weeks. Arterial pressure was higher (p<0.01) in obese
rats fed 4% NaCl (130±4 mm Hg) than in obese rats fed 1% NaCl (118±2 mm Hg) or than in lean rats
fed either NaCl intake (118±3 mm Hg and 116±3 mm Hg, respectively). Cardiac output of obese rats
was higher than that of lean rats (/xO.Ol); however, the NaCl-induced increase of blood pressure was
accounted for by an increase of peripheral resistance (p<0.01). Thus, in contrast to the lean Zucker
rat, arterial pressure of the obese Zucker rat is increased by a high dietary intake of NaCl.
(Hypertension 1992^0-389-393)
KEY WORDS • sodium, dietary • obesity • cardiac output • vascular resistance • blood pressure
• rats, Zucker
n humans, hypertension is associated with obesity.1
Obesity-related hypertension has been ascribed to
hypervolemia and an increased cardiac output without an appropriate reduction of peripheral resistance2 and
to increased sympathetic nervous system activity.3 Further, it has been suggested that insulin resistance associated with obesity contributes to hypertension.4
The Zucker fatty rat inherits obesity as an autosomal
recessive trait.3 Rats homozygous for the fatty gene are
also insulin resistant and hyperinsulinemic. Based on
indirect, tail-cuff measurements and direct measurement of intra-arterial pressure, several reports have
indicated that blood pressure of the obese Zucker rat
does not differ from that of lean controls.6-10 In contrast, other reports have indicated that arterial pressure
is increased in this animal model.11-15 One purpose of
the present study was to compare measurements of
arterial pressure, cardiac output, and peripheral resistance in obese Zucker rats and lean controls.
In the human, there is some evidence that obesityrelated hypertension is salt sensitive.16'17 Consequently,
we hypothesized that blood pressure in this rat model of
obesity would be increased by a high NaCl intake. In the
present study, arterial pressures were compared in
I
From the Department of Medicine, West Virginia University,
School of Medicine, Morgantown, W.Va.
Supported in part by grant HL-37753 from the National Heart,
Lung, and Blood Institute, National Institutes of Health, Bethesda,
Md.
Address for correspondence: Theodore A. Kotchen, MD, Department of Medicine, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, Wl 53226.
Received December 10,1991; accepted in revised form April 27,
1992.
obese and lean Zucker rats on normal and high NaCl
intakes.
Methods
In protocol 1, we evaluated the effect of a high NaCl
intake in obese and lean rats by measuring indirect
blood pressures in the tail. In protocol 2, direct arterial
pressures and cardiac outputs were measured in separate groups of chronically instrumented, conscious
obese and lean rats fed either a normal or a high NaCl
diet.
For both protocols, lean and obese female Zucker
rats were purchased from Harlan Sprague Dawley, Inc.,
Indianapolis, Ind., shortly after weaning at age 4 weeks.
The rats were housed in individual metabolic cages in a
temperature- (22°C) and light-controlled (12-hour
light/dark cycle) small animal facility. All rats ate and
drank ad libitum, and body weights were measured
twice weekly.
In protocol 1, lean and obese rats were fed chow
containing 0.45% NaCl (TD 88311, Teklad, Madison,
Wis.) and were given either distilled water or 0.9%
NaCl (n=5-6 per group) to drink for 18 days. For the
measurement of indirect arterial pressure, twice weekly,
rats were placed in a heated rodent restrainer (Harvard
Apparatus, South Natick, Mass.) and were maintained
at a constant temperature of 39°C, beginning 15-20
minutes before the measurement. For each data point,
nine tail-cuff measurements were obtained with a pneumatic pulse transducer (Narco BioSystems, Austin,
Tex.), a pressure transducer (P23-ID, Gould Electronics, Cleveland, Ohio), and a polygraph (model 7D,
Grass Instrument Co., Quincy, Mass.). The first two
readings and the highest and lowest remaining readings
390
Hypertension
Vol 20, No 3
September 1992
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were discarded. The remaining five readings were averaged to obtain each data point. The observer reading
the blood pressure recordings was unaware of the group
assignment of the rats.
In protocol 2, separate groups of 4-week-old lean and
obese Zucker rats were placed on either a 1% NaCl diet
(Purina chow) or a 4% NaCl intake, prepared by adding
NaCl to Purina chow (n = 13-15 rats in each diet-strain
group). After remaining on these diets for 12 weeks,
direct intra-arterial pressures were measured in all rats
in the conscious, unrestrained state. Cardiac outputs
were measured in 7-9 rats in each diet-strain group,
and after the measurement of arterial pressure, hearts
were dissected and weighed in the remaining six rats in
each group.
As we have previously described18 for measurement
of cardiac output, the left carotid artery was catheterized with a thermistor-catheter combination. The right
jugular vein was catheterized with Tygon microbore
tubing (0.015 inch i.d.xO.030 inch o.d.), and the catheter was advanced into the right atrium. In those rats not
undergoing measurement of cardiac output, a carotid
artery was catheterized with a Tygon microbore catheter (0.24 inch i.d.x 0.040 inch o.d.). In all instances, rats
were chronically instrumented with catheters that were
inserted under Brevital anesthesia (40 mg/kg i.p.). After
catheter placement, rats were treated with a single
intramuscular dose of penicillin G (20,000 units) and
streptomycin (25 mg). Catheters were tunneled subcutaneously to exit at the base of the skull. All measurements of direct arterial pressure and cardiac output
were carried out at least 3 days after preparatory
surgery.
For measurement of cardiac output, a 100 -fil bolus of
room temperature (18-19°C) 5% dextrose was injected
into the jugular venous catheter with a Hamilton dispensing pipette fitted into an automatic dispensing
device. The temperature of the injectate was measured
with a platinum-tipped thermometer that was accurate
to 0.2cC, and temperature change of the blood was
measured with the precalibrated indwelling thermistor.
The outputs of both the thermometer in the injectate
and the aortic thermistor were recorded with a Cardiomax thermistor microprobe coupled to a thermodilution
cardiac output computer (Cardiomax II, model 58,
Columbus Instruments, Columbus, Ohio). Three 100-fil
injections were performed, and the average cardiac
output was computed. Total peripheral resistance
(TPR) was calculated by dividing the simultaneously
obtained arterial pressure by cardiac output
Statistical significance of differences between obese
and lean rats on each of the two diets was determined
with a two-factor (strain and diet) analysis of variance.
Where statistically significant, overall differences were
observed; specific group differences were identified with
the least significant differences test. Results are presented as mean±SEM.
Results
Protocol 1: Indirect Blood Pressure Measurements
At the completion of the study, the mean weight of
obese rats (255±4 g) was greater (/?<0.001) than that of
lean rats (140 ±3 g). Dietary NaCl intake did not affect
weight gain in either group. Salt intake also did not
1 tU
120
1
1
1
1—
OBESE
100
E
80
T/Y
O Water
• 0.9X NaCl
60 -
1
,
1
1
1
10
15
20
140
LEAN
120
e
E
100
O Water
• 0.9% NaCl
80
60
0
5
10
15
20
DAY ON DIET PROTOCOL
FIGURE 1. Line graphs show systolic blood pressure in obese
and lean Zucker rats drinking either 0.9% NaCl solution or
water.
affect blood pressure in the lean rats; however, NaCldrinking obese Zucker rats had significantly higher
blood pressures (p<0.05) than water-drinking obese
rats (Figure 1). Blood pressures in the water-drinking
obese rats did not differ from those in the lean rats.
Protocol 2: Direct Arterial Pressure, Cardiac Output,
and Peripheral Resistance
Within each strain, weight gains in the rats on the two
N a d intakes were similar, and at the completion of the
study, mean body weight of obese rats was approximately two times that of lean rats (Table 1). Among
obese and lean rats, body weights did not differ significantly on the two NaCl intakes. Further, among the
obese rats, the heart weight-to-body weight ratio was
higher (/><0.01) in rats on the 4% NaCl intake than in
those on the 1% NaCl intake. The heart weight-tobody weight ratio was not affected by NaCl intake in the
lean animals. On the 1% NaCl intake, direct mean
intra-arterial pressures of obese and lean animals did
not differ (Figure 2). However, arterial pressure was
significantly higher in obese rats on the 4% NaCl intake
than that in obese rats on the 1% NaCl intake (/?<0.01)
or that in lean animals on either NaCl intake (p<0.01).
Arterial pressure was not affected by N a d intake in
lean animals.
Cardiac output was higher (/?<0.0001) in obese than
in lean rats. Among obese rats, cardiac output was lower
(p<0.01) and TPR was higher (/><0.01) in those fed
the 4% NaCl than in those fed the 1% NaCl diet.
Reddy and Kotchen
NaCI and Blood Pressure in the Obese Rat
391
TABLE 1. Mean Body Weight, Heart Wdght-to-Body Weight Ratio, and Hemodynamic Measurements in Obese and Lean Rats Fed 1% or 4% NaCI Diet for 12 Weeks
Obese
l%Nad
426±12
Lean
4%NaCl
403 ±10
Body weight (g)
Heart weight
•>
1.70±0.06
2.09±0.07*
—xlO~3
Body weight
130±4*
118±2
Mean arterial pressure (mm Hg)
191±6
171±5*
Cardiac output (ml/min)
0.74±0.03*
0.62±0.03
TPR (mm Hg • ml"1 • min"1)
TPR, total peripheral resistance. Values are mean±SEM.
•p<0.01 compared with obese rats fed 1% Nad.
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Among lean rats, cardiac output and TPR did not differ
significantly between those on the two NaCI intakes.
Because of their greater body weight, cardiac index of
obese rats was less than that of lean rats (/7<0.001). In
both strains, cardiac index was not significantly affected by
NaCI intake. Consequently, the computed TPR based on
cardiac index (rather than cardiac output) was higher in
obese than in lean rats (p<0.01). However, among obese
rats, similar to results based on cardiac output, TPR
computed on the basis of cardiac index was also higher
(p<0.03) in those on the 4% N a d intake (3.03±0.11
mm Hg • ml"1 • muT1 • 100 g"1) than in those on the 1%
NaCI intake (2.72±0.12 mmHg-mr'-min- 1 • 100 g"1);
TPR was not significantly affected by NaCI intake in lean
rats.
Discussion
In the conscious animal, both indirect and direct
intra-arterial pressures did not differ in Zucker obese
and lean rats on a "normal" NaCI intake, although
cardiac output was higher and TPR was lower in obese
animals. Blood pressures were increased by a high NaCI
intake in obese but not in lean animals, and the
NaCl-induced elevation of blood pressure was due to an
increased TPR.
135
1
w
X
•n
w
K
a,
130
|^|
1 Obese
Lean
CO
125 QO
£ 120
T
JU T
115
%
w
-
110
s
105
100
-
m
1•
11
DIET: 1% NaCI
4% NaCI
• p< 0.01 compared to all other groups
FIGURE 2. Bar graph shows direct arterial pressure in obese
and lean Zucker rats on normal or high NaCI intakes.
l%Nad
210±4
4% N a d
208+4
2.78±0.08
2.87+0.05
116±3
129±3
0.87±0.03
118+3
129+3
0.91+0.03
Previous studies have indicated that hypertension is
not consistently associated with obesity in the rat.
Results in the obese Zucker rat are conflicting.6-15
Obesity-inducing lesions of the ventromedial hypothalamus either have no effect on blood pressure or result in
hypotension, and these lesions prevent the developmentof hypertension in several experimental models.19-22
However, these lesions also decrease sympathetic outflow. Blood pressures have been reported to be normal23
or slightly elevated24-25 in rats with obesity induced by
programming the animals to eat a high fat diet. Based
on indirect tail-cuff measurements, it has been reported
that blood pressure in obese spontaneously hypertensive rats (SHR) is lower than in nonobese littermates.26^7 The only obese rat model with persistent
hypertension was originally developed by Koltetsky,
who bred rats that were spontaneously hypertensive
with genetic traits for obesity.28
There is little information in the literature concerning
salt sensitivity of blood pressure in the obese rat. Pawloski
et al29 have recently reported that a continuous intravenous sodium infusion (6 meq sodium per day) for 1 week
did not significantly increase blood pressure in a small
group (n=5) of obese Zucker rats. However, Kasiske et
al30 reported that tail systolic blood pressures were significantly but modestly increased in obese Zucker rats fed
standard chow supplemented with 4% N a d for 22 weeks,
but not for 8 weeks. The high NaCI intake did not affect
blood pressure in lean rats.
Although blood pressure of the Dahl salt sensitive
(Dahl-S) rat is more salt sensitive than the obese Zucker
rat, similar mechanisms may account for salt sensitivity
of blood pressure in both models. Similar to the present
observations in the obese Zucker rat, NaCl-induced
elevations of blood pressure in the Dahl-S rat are also
due to an increase of TPR.18 Fat-fed obese rats and
Dahl-S rats have augmented vasoconstrictor responses
to pressor agents.31-32 An impairment of arterial baroreceptor reflex activity has been implicated in the salt
sensitivity of blood pressure in the Dahl-S rat.33-38
Baroreceptor reflex control of heart rate is also impaired in the obese Zucker rat7 and in the obese Wistar
rat maintained on a high fat diet.24 In both the Dahl-S
rat and the obese Wistar rat, the decreased baroreceptor reflex control of heart rate appears to be due to an
impairment in the parasympathetic limb of the reflex.7-21
In contrast, arterial baroreceptor reflex control of heart
rate is not reduced in the obese, fat-fed dog.39
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Hypertension
Vol 20, No 3 September 1992
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Sympathetic tone is also increased in the Dahl-S rat
and in the SHR fed a high-NaCl intake.18"0-41 However,
sympathetic tone is actually decreased in the obese
Zucker rat, as demonstrated by decreased release of
norepinephrine from nerve terminals in response to
stress.42 Conceivably, reduced sympathetic tone may
account for the relatively modest effect of dietary NaCl
on blood pressure in this rat model of obesity.
Obesity is associated with resistance to insulin-stimulated glucose uptake and hyperinsulinemia.4 We have
recently demonstrated that the Dahl-S rat is also insulin
resistant, whereas the one-kidney, one clip hypertensive
rat and the two-kidney, one clip hypertensive rat are
not.43-44 Insulin resistance has also been observed in
the SHR 45 and in human hypertension46-48; in hypertensive humans, insulin resistance appears to be associated with salt sensitivity of blood pressure.49-50 Consequently, insulin resistance may contribute to the salt
sensitivity of blood pressure in the obese Zucker rat.
In conclusion, blood pressure of the obese Zucker rat
is increased by a high dietary intake of NaCl. Similar to
earlier observations in the Dahl-S rat, the NaCl-induced
elevation of blood pressure is accounted for by an
increased TPR. We hypothesize that similar mechanisms
account for the NaCl-induced elevation of arterial pressure in both the obese Zucker rat and the Dahl-S rat.
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Dietary sodium chloride increases blood pressure in obese Zucker rats.
S R Reddy and T A Kotchen
Hypertension. 1992;20:389-393
doi: 10.1161/01.HYP.20.3.389
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