Influence of oat bran of sucrose-induced blood pressure elevations in SHR

Life Sciences, Vol. 47, pp. 1121-1128 Printed in the U.S.A.

INFLUENCE

Pergamon Press

OF OAT BRAN ON SUCROSE-INDUCED ELEVATIONS IN SHR

BLOOD PRESSURE

Mohmed el Zein Jorge Areas , Joseph Knapka , Gilbert Gleim, Donald DiPette , Bryan Holland , and Harry G.Preuss l)Department of Medicine (Nephrology) & Pathology Georgetown University Medical Center, Washington, D.C., 20007 ; 2) Division of Research Services, National Institutes of Health, Bethesda, MD 20306; 3) Nicholas Institute of Sports Medicine & Trauma, Lenox Hill Hospital, New York, N.Y, 10021 and 4) Department of Medicine (Endocrinology, M e t a b o l i s m & Hypertension) U n i v e r s i t y of Texas Medical Branch, Galveston, TX, 77550 (Received in final form July 23, 1990) Summary To determine whether oat fiber influences BP, we gave spontaneously hypertensive rats (SHR) a diet high in sucrose and low in protein (calories: sucrose 52%, protein 15%, fat 33%) or a diet low in sucrose and high in protein (calories: sucrose 13%, protein 52%, fat 35%). The amount of fat in these particular diets has not been shown to influence BP, so we modified the 2 diets by replacing fat with oat bran (10% w/w). Accordingly, we examined 4 groups of 5 rats consuming different diets:high sucrose, high sucrose + oat bran, low sucrose, and low sucrose + oat bran. Not unexpectedly, SHR consuming the diet high in sucrose had a significantly higher BP after 2 weeks than those consuming the diet low in sucrose. The significant difference in BP continued over the next 3 weeks. At the end of 6 week duration of study, we found the following BP: SHR ingesting the high sucrose diet, 217 mm Hg ~ 5 (SEM) vs SHR consuming the low sucrose diet, 187 mm Hg ~ 4 (SEM) p<.0001]. SHR eating the low sucrose diet and consuming supplemental bran showed no significant change in BP after 6 weeks compared to SHR eating the basic diet alone, 188 mm Hg ± 6 (SEM); however, 5 SHR consuming the high sucrose diet with added oat bran showed a significantly lower BP 200 mm Hg ~ 2 (SEM) than SHR ingesting the basic high sucrose diet devoid of oat bran [p<.01]. We conclude that addition of oat bran to the diet can ameliorate sucrose-induced BP elevations in SHR. The ingestion of dietary fiber may influence blood pressure (BP). It has been suggested that fiber in the diet of vegetarians plays a role, at least to s o m e extent, in their lower BP (i). Several reports also suggest that increasing fiber intake lowers BP of normotensive and hypertensive individuals (2-4). However, the various diets used to gather this * To whom correspondence

should be sent

0024-3205/90 $3.00 + .00 Copyright (e) 1990 Pergamon Press plc

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Oat Bran and Blood Pressure

Vol. 47, No. 13, 1990

information differ in many factors other than the quantity and quality of fiber (5). Accordingly, it is difficult to pinpoint the exact role of fiber in regulating BP. Recently, we examined the effects of different diets containing only refined ingredients on the BP of spontaneously hypertensive rats (SHR) (6). The most consistent observation was that the diets high in sucrose and other refined carbohydrates, whether they replaced proteins or fats, significantly increased BP. As a first approximation, the present study was designed to ascertain whether adding oat bran containing roughly 20% fiber to diets consisting of only refined ingredients would affect the BP response. Materials

& Methods

Twenty SHR (Charles River, MA), weighing between 190 and 240 g, were obtained for this short-term study. All rats initially were fed rat chow (Purina) ad libitum. During the study, the rats were housed 2-3 per cage and baseline BP were measured using tail plethysmography. After 2 weeks of acclimatization, a baseline weight and BP were recorded, then SHR were divided into 4 groups of 5 rats each, and each group was randomly assigned to be fed one of the 4 experimental diets. The four diets examined in this study are listed in table i. The diet designated as high sucrose had the largest percentage of energy contributed by sucrose (52%) while protein contributed the smallest percentage of the total calories (15%). The CHO fraction contributed the lowest percentage of calories in the low sucrose diet (13%) while the highest percentage was contributed by the protein fraction (52%). The two additional diets were modified by replacing 10% w/w of fat with oat bran. The amount of vitamins and minerals added to each diet was kept essentially the same. Therefore, we had 5 rats consuming one of 4 diets: High Sucrose, High Sucrose + Oat Bran, Low Sucrose, and Low Sucrose + Oat Bran. Body weight, urinary output, creatinine, Na and K excretion were measured by standard methods (6). Two urine collections were made in the last week of study. The rats were placed in individual metabolic cages for 24h. The first urine was collected without preservatives for electrolyte and creatinine analysis. In the second, urine for catecholamine assays were collected in a known volume of perchloric acid to preserve catecholamines and frozen for subsequent analyses of creatinine and catecholamine concentrations. Creatinine was estimated using an alkaline picrate method (7). The concentrations of urinary norepinephrine, epinephrine, and dopamine excreted were determined using a radioenzymatic assay (8). BP measurements were by tail plethysmography as described previously (6). Excessive heating had to be avoided, because the SHR is heat sensitive (9). Approximately, 6-7 readings were taken one minute apart, and the lowest reproducible reading was accepted as the systolic pressure. After the experimental diets were fed for 6 weeks, the rats were anesthetized with methoxyflurane and blood was drawn from

Vol. 47, No. 13, 1990

Table

Oat Bran and Blood Pressure

1 - Formulations

High Sucrose

Ingredient

Casein

of the Experimental

P e r c # n t a g e i n Weight High Sucrose + Oat Low Bran Sucrose

1123

Diets

Low Sucrose + Oat Bran

15.0

15.0

58.2

58.2

D1-Methionine

0.2

0.2

0.8

0.8

Sucrose

61.3

61.3

15.0

15.0

Corn Oil

5.0

5.0

5.0

5.0

13.0

3.0

15.0

5.0

Hydrogenated

Oil

AIN Mineral mix

(+) 4.1

4.1

4.4

4.4

AIN Vitamin mix

(+) 1.2

1.2

1.3

1.3

0.2

0.2

0.3

0.3

0

10.0

0

10.0

i00.0

i00.0

i00.0

Choline Oat Bran

bitartrate

100.0

+ American Institute of Nutrition, 1977, Standards for Nutritional Studies Report J Nutr 107:1340.

Ad Hoc Committee on of the Committee.

the lower aorta for chemistry assays. Blood for renin assays was collected separately in cold tubes containing known amounts of EDTA. Plasma renin activity was measured by RIA (Biotecx, Friendswood, TX). After the blood was obtained, the anesthetized rats were sacrificed by giving a solution used for euthanasia (T 61). The heart and kidneys were removed, cleaned, and weighed. Two-way analyses of variance and Dunnett's multiple range test were performed using the Statview 512 Plus System on a Macintosh computer. If the results of the statistical analyses demonstrated a P<0.05, they were considered to be statistically significant. Results Body Weight (Fig. i): The body weight of the rats fed the low sucrose diets (with and without oat bran) tended to be lower although not significantly different than rats consuming the high sucrose diets(with and without oat bran). Compared to the basic diet, the addition of oat bran did not seem to influence body weight markedly.

1124

Oat Bran and Blood Pressure

360.

~ --

e--

Vol. 47, No. 13, 1990

High Sucrose High Sucrose + Oat Bran

"r [

Low Sucrose - - m- -

Low Sucrose + Oat Bran

T

340.

.

:

320.

12 0

r~

s ~-

. . . . . . . . . . . . . . . .

5

10

lS

20

2$

30

35

40

DAYS

FIGURE 1 Change in body w e i g h t of SHR c o n s u m i n g the diets over the course of 6 weeks. Average SEM of 5 rats in e a c h group is depicted.

4 ±

B l o o d P r e s s u r e (Fig. 2): F r o m the second to third w e e k of study, the change in BP above b a s e l i n e (~BP) of the rats c o n s u m i n g the h i g h s u c r o s e diets rose s i g n i f i c a n t l y above those i n g e s t i n g the low s u c r o s e diets w h e t h e r oat b r a n was added or not. However, s o m e t i m e after the third week, the rats c o n s u m i n g the h i g h s u c r o s e d i e t c o n t i n u e d to s h o w a rise in BP w h i l e the BP of those w i t h a d d e d oat b r a n b e g a n to level off. Thus, over the last 3 w e e k s of the study, the SHR c o n s u m i n g the h i g h sucrose diet s h o w e d a h i g h e r BP than those i n g e s t i n g the h i g h sucrose diet w i t h a d d e d oat bran. In turn, b o t h these groups s h o w e d s i g n i f i c a n t l y h i g h e r BP than the rats c o n s u m i n g the low s u c r o s e diets. The final a v e r a g e BP of e a c h g r o u p at the end of the s t u d y was as follows: h i g h sucrose, 217 m m Hg ± 4.6 (SEM); h i g h s u c r o s e + oat b r a n , 2 0 0 m m Hg ~ 1.6 (SEM); low sucrose, 187 m m Hg ~ 4.0 (SEM); low s u c r o s e + oat bran, 188 m m Hg ~ 6.3 (SEM). U r i n a r y M e a s u r e m e n t s (Table 2): The e x c r e t i o n of Na was h i g h e r in the rats i n g e s t i n g the h i g h sucrose diet w h e t h e r oat b r a n was p r e s e n t or not. P o t a s s i u m and c r e a t i n i n e e x c r e t i o n w e r e similar a m o n g the groups. E p i n e p h r i n e e x c r e t i o n was s i g n i f i c a n t l y e l e v a t e d in the SHR c o n s u m i n g h i g h sucrose, and the p r e s e n c e of oat b r a n did not alter the results. W h i l e the t e n d e n c y was for n o r e p i n e p h r i n e e x c r e t i o n to be h i g h e r in the 2 groups c o n s u m i n g h i g h sucrose, the d i f f e r e n c e s w e r e not s t a t i s t i c a l l y s i g n i f i c a n t l y different. D o p a m i n e e x c r e t i o n levels w e r e not d i f f e r e n t among the 4 groups. Blood p a r a m e t e r s (Table 2): Other t h a n serum u r e a n i t r o g e n (SUN) w h i c h was s i g n i f i c a n t l y lower in the rats ingesting the h i g h sucrose diets, the other p a r a m e t e r s such as Na, K, CI, CO2, glucose c r e a t i n i n e and m a g n e s i u m were e s s e n t i a l l y similar. Plasma renin a c t i v i t y (PRA) was g e n e r a l l y higher in the rats c o n s u m i n g oat b r a n w h e t h e r w i t h the h i g h or low sucrose diet.

47, No.

Vol.

Oat B r a n and B l o o d P r e s s u r e

13, 1 9 9 0

Table

2

-

1125

Various Parameters in SHR on High & Low Sucrose Diets with and without Oat Bran

~Parameter Urine

High Sucrose

High Sucrose + Oat Bran

Low Sucrose

Low Sucrose + O~t Bra~

Vol (ml/24h)

3.3 ±

0.7

2.7 ±

0.4

3.6 ±

0.3

4.7 _

0.5z

Na (mEq/24h)

0.54 ±

0.07

0.43 ±

0.09

0.19 ±

0.03u

0.17 ±

0.05u

K (mEq/24h)

0.59 ±

0.08

0.49 ±

0.09

0.50 ±

0.03

0.55 ±

0.04

Creatinin¢ (mg/24h)

7.5 ±

0.4

6.1 ±

1.1

7.0 ±

03

7.0 ±

0.3

Norepinephrlne (ng/24h)

Epinephrine

116

±

10.4

111

±

35

-+

4.3

41

_+

10

4.8

101

±

8.8

93

+-

3.3

22

±

2.3u

23

_

1.6z~

(ng/24h) Dopamine (ng/24h)

453

± 128

323

± 24

403

± 91

275

± 26

144

+

1.0

143

+

0.9

144

+

0.5

142

+

5.0 +

0.1

5.3 +

0.1

5.0 +

0.2

Blood Na (mEq/L) K (mEq/L) (31 (mEq/L) CO= (mEq/L) Glucose (mg/dl) SUN (mg/dl)

107

+

18.9 +

1 0.7

106

+

19.2 +

1

0.8

154

+

8.8

153

+

7

12

+

0.4

12

+

0.8

107

+

18.2 +

i

0.2

158

+

3

28

+

2.5I~

5.1 + 106

+

18.1 +

.05 0.3 1

1.0

148

+

8.3

31

+

4.2m

Crcatinln¢ (mg/dl)

0.65 +

.03

0.60 +

0.02

0.63 +

0.03

0.58 +

0.03~

Mg (mEq/L)

2.0 +

0.07

2,o +

0.02

2,0 +

0.09

2.1 +

0.06

3.7 +

0.5

7.5 +

0.7 l

4.7 +

0.5

7.2 +

1.8'

PRA HCT

(.gl,.I/h) (%)

44

+

0.7

45

+

0.6

46

+

1.7

48

+

2.4

Miscellaneou~ Right Kidney (g)

L30 +

0.09

136 +

0.05

1.56 +

0.1

1.53 +

0.07

Heart wt (g)

1.33 +

0.01

139 +

0.04

1.39 +

0.07

1.38 +

0.08

1 2

Significantly different from column 1 Significantly different from column 2

1126

Oat Bran and Blood Pressure

225 -"

Vol. 47, No. 13, 1990

----0--

High Sucrose

--

0------{3---

High Sucrose +Oat Bran Low Sucrose

--m--

Low Sucrose + Oat Bran

d ~ B B ~ m

215

205

E

v E

195

0.

185

.,Li 175

165

. . . .

0

i

5

. . . .

i

10

. . . .

!

15

. . . .

!

. . . .

20

I

25

. . . .

i

30

. . . .

!

35

. . . .

i

,

,

40

DAYS

FIGURE 2 C h a n g e in b l o o d p r e s s u r e of SHR c o n s u m i n g the 4 d i e t s o v e r the c o u r s e of 6 weeks. A v e r a g e ± SEM of 5 rats in e a c h g r o u p is d e p i c t e d . + S i g n i f i c a n t l y d i f f e r e n t from low sucrose diet, # S i g n i f i c a n t l y d i f f e r e n t f r o m low sucrose diet, low s u c r o s e d i e t + oat b r a n * S i g n i f i c a n t l y d i f f e r e n t f r o m low sucrose diet, low sucrose + oat b r a n and h i g h sucrose + oat bran. Discussion We k n o w that the a d d i t i o n of h i g h c o n c e n t r a t i o n s of s u c r o s e or o t h e r r e f i n e d c a r b o h y d r a t e s to the d i e t s of rats i n c r e a s e s BP (6,10). The SHR are v e r y s e n s i t i v e to the e f f e c t s of h e a v y s u c r o s e i n g e s t i o n s h o w i n g a rise of BP a p p r o x i m a t e l y 15-25 m m Hg o v e r a 2-3 w e e k p e r i o d (11,12). The e t i o l o g y of this e f f e c t m a y a r i s e f r o m m u l t i p l e causes. A m o n g the m a n y p o s s i b i l i t i e s , s u c r o s e m a y c a u s e this rise in BP t h r o u g h its e f f e c t s on c a t e c h o l a m i n e m e t a b o l i s m , c i r c u l a t i n g volume, a n d / o r a c i r c u l a t i n g f a c t o r a f f e c t i n g m e m b r a n e t r a n s p o r t (ii). P r e l i m i n a r y c l i n i c a l s t u d i e s u s i n g p l a n t f i b e r a n d / o r bran, e s p e c i a l l y that o b t a i n e d f r o m oats, have i n d i c a t e d that those c o n s t i t u e n t s m a y p r o d u c e a s i g n i f i c a n t e f f e c t on BP (2-5). H o w e v e r , it is d i f f i c u l t to be c e r t a i n that the a b o v e are d i r e c t l y r e s p o n s i b l e for the e f f e c t since o t h e r c o n s t i t u e n t s of the diet, i.e., m a c r o n u t r i e n t s and m i c r o n u t r i e n t s , were not adequately controlled. R e c e n t l y , we a t t e m p t e d to limit the above o b j e c t i o n s by f o r m u l a t i n g d i e t s for r a t s w h e r e only the p r o p o r t i o n s of m a c r o n u t r i e n t s such as CHO, p r o t e i n and fat v a r i e d significantly. By u s i n g those diets, we found that a d d i t i o n of

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Oat Bran and Blood Pressure

1127

sucrose, whether it replaced protein or fats, caused significant rises in BP (6). Therefore, the BP elevation is due to the high sucrose ingestion rather than the lack of protein or fat in the diet. Because the amount of fat in these refined diets did not influence BP (6), we replaced fat with oat bran in the present study to determine how the latter would affect BP, especially the elevation produced by sucrose. As a first approximation, we selected only one concentration of oat bran to be examined (10% w/w); and this significantly ameliorated, the sucrose-induced BP rise. Interestingly, the presence of oat bran did not significantly influence the BP of SHR consuming low sucrose diets. Therefore, the diet being consumed is important in determining whether oat bran plays some role in pressure regulation. Since the basic diets of humans ingesting bran or fiber in previous studies have not been precisely controlled in all situations, this may explain the variable responses reported (5). We hasten to add that the present studies do not tell us if the addition of a higher concentration of oat bran and/or fiber to the diets could have completely overcome the sucrose-induced rise in BP. Also, the design of the study does not permit us to speculate on the effects of other brans. Because of previous reports, we assume that the soluble fiber in the oat bran is producing our effect. It is possible, although we believe unlikely, that the digestable, non fiber components of oat bran have caused the differences. Nevertheless, oat bran does influence sucrose-induced BP elevations. Some potential mechanisms through which oat bran can reduce BP are effects on the rate of nutrient and water absorption from the intestinal lumen, reduction in insulin production, and changes in the secretion of glucagon and glucocorticoids as well as various gastrointestinal, vasoactive polypeptides (4,5). In our study we know that differences in body weight and electrolytes are not the basis, because they were not significantly different in the high sucrose rats receiving or not receiving bran in their diets. In the past we have suggested that catecholamine metabolism and/or alterations in blood volume are involved in sucrose-induced hypertension. Our results did not indicate that either of these mechanisms were involved in the BP changes following bran ingestion. Oat bran could lower circulating volume by increasing fecal water loss to produce its effect of BP (5). The higher levels of PRA in the high sucrose SHR consuming oat bran compared to those not receiving oat bran are consistent with this possibility. Acknowledgments Supported by NIH grant AG 06929. The authors wish to acknowledge the excellent secretarial assistance of Mrs. Elizabeth Ergueta. We wish to commend Mr. Ronald Rose of the Teklad Corporation, Madison, WI, for his helpful advice in devising our diets and the National Oat Company, Cedar Rapids, Iowa, for their generous donation of the oat bran. We also wish to acknowledge the help of Ms. Renee Swanson, a recipient of a summer traineeship from the American Heart Association.

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Oat Bran and Blood Pressure

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References I.

2.

4.

5. 6. 7.

8.

9. i0. ii. 12.

B. ARMSTRONG, A.J. VAN MERWYCK and H. COATES. Am J Epidem. 105, 444-449 (1977). H. DIEHL and D. MANNERBERG. In: H.C. Trowell, D.P. Burkitt, eds. Western Diseases: Their Emergence and Prevention. London: Edward Arnold, 392-410 (1981) P. DOPSON and D. HUMPHREYS, In: H.C.Trowell D.P. Burkitt eds. Western Disease: Their Emergence and Prevention. London: Edward Arnold, 411-420 (1981). A. WRIGHT, P.G. BURSTYN and M.J. GIBNEY, British Med J 2,1541-1543 (1979). J. W. ANDERSON, Annals of Int Med. 98, 842-846 (1983). M. ZEIN, J. AREAS, J . KNAPKA, D. DIPETTE, B. HOLLAND and H.G. PREUSS, Am J Hyper ~:380-386, (1990). R.A. PHILLIPS , In Quantitative Clinical Chemistry Methods (Army ed), J.P. Peters and D.D. Van Slyke. Eds.,Battermore MD, Williams and Wilkins, Vol 2, 604a (1944). M.N. HUSSAN and C.R. BENEDIT, Clin Chem 3!I,1861-1864 (1985) J.M. PFEFFER,M.A. PFEFFER and E.D. FROELICH, J Lab Clin Med 78, 957-962, (1971). H.G. PREUSS, R.D. FOURNIER, J. PREUSS, M. ZEIN, C. GARCIA and J.KNAPKA, J Clin Biochem Nutr. 5,9-20 (1988). M.B. PREUSS and H.G. PREUSS,Lab Invest. 4--3,101-107 (1980) H.G. PREUSS and R.D. FOURNIER, Life Sci. 3--0,879-886 (1982).