Plasma Cholesterol Concentrations in African Grey Parrots Fed Diets Containing Psyllium

F. J. Bavelaar, MVR, MSc

A. C. Beynen, Prof. Dr. Ir.

Department of Nutrition

Faculty of Veterinary Medicine

University of Utrecht, Utrecht,

The Netherlands

Key words: African grey parrots, psyllium, plasma cholesterol concentrations

Abstract

The incidence of atherosclerosis in African Grey parrots is high. An important risk factor for atherosclerosis in humans is an elevated plasma cholesterol concentration; this might also hold for parrots. We have shown earlier that plasma cholesterol levels in African Grey parrots can be lowered by a decrease in the intake of saturated fatty acids or an increase in the intake of polyunsaturated fatty acids. In humans, as in experimental animals, the ingestion of psyllium has a hypocholesterolemic effect. Therefore, in this study, we evaluated the influence of dietary psyllium in African Grey parrots. The diets contained either cellulose 3.22% or 6.44 % psyllium; the control and test fibers were exchanged on a weight basis. Three groups, with a total of 16 animals, were fed the experimental diets according to a 3 ¥ 3 Latin-square design with feeding periods of 28 days. No psyllium effect was found on plasma cholesterol concentrations. The unexpected lack of hypocholesterolemic effect for psyllium ingestion cannot be explained by an insensitivity of plasma cholesterol to diet composition because the parrots used had been shown earlier to respond to the type and amount of dietary fat. Moreover, the lack of effect is not explained by type of psyllium preparation, low dosage, short duration of feeding, use of cholesterol-free diets, or insufficient statistical power. We suggest that the addition of psyllium to the diet mixtures in dry form or the extrusion process diminished the hypocholesterolemic activity. In any event, under the present experimental conditions, dietary psyllium did not affect plasma cholesterol in African Grey parrots.

Introduction

Atherosclerosis is common among parrots, especially among African Grey parrots and Amazons.1–4 The etiology of atherosclerosis in parrots is not known; however, one of the most important risk factors of atherosclerosis in humans is an elevated plasma cholesterol concentration.5 An high plasma cholesterol concentration is also associated with atherosclerosis in birds such as quails6,7 and budgerigars.8 A high plasma cholesterol concentration is probably a risk factor for atherosclerosis in parrots as well. Cholesterol can be changed through dietary intervention, not only in humans5 but also in parrots. Bavelaar and Beynen9 showed that plasma cholesterol levels can be lowered by feeding a diet either rich in polyunsaturated fatty acids or low in fat.

Researchers recognize that dietary soluble, viscous fibers such as pectin and psyllium can lower plasma cholesterol concentrations in humans, guinea pigs, chickens, hamsters, and rats.10–13 Psyllium is prepared from the husk of seeds from Plantago ovata and consists of approximately 85% mucilage and 15% nonpolysaccharide components.14 It is not known whether dietary psyllium affects plasma cholesterol concentrations in parrots. To assess the cholesterolemic effect of psyllium in African Grey parrots, 18 birds were fed diets containing either psyllium or cellulose as nonsoluble, control fiber. The experimental design was a 3 ¥ 3 Latin square so that two dietary concentrations of psyllium were tested.

Materials and Methods

Animals and housing

A total of 18 African Grey parrots (Psittacus erithacus) were studied. The parrots were made available by the Dutch Parrot Refuge (Nederlandse Opvang Papegaaien, Veldhoven, The Netherlands). The parrots were of both genders, with ages ranging from 3 to 32 years and body weight from 347 to 550 g. Three dietary groups were formed, two groups of 7 birds each and one group of 4 birds. Two groups were each housed in a single aviary and the third group was divided over two aviaries. The parrots had been chipped for identification. The aviaries had an indoor and outdoor space. Outside, the floor was covered with sand and inside with wood shavings. Indoors, there was continuous light as is common practice in the parrot center. Feed and water were provided inside for ad libitum consumption and were refreshed daily. The aviaries were cleaned weekly. Food consumption was recorded for each aviary. At the end of each dietary period, all parrots were caught for collection of blood samples and determination of body weight. If a parrot had lost 15% or more of its initial body weight, it was excluded from the experiment because such a degree of weight loss endangers the health of parrots.

Experimental Design

The experiment was approved by the animal experiments committee of the Faculty of Veterinary Medicine, Utrecht, The Netherlands. The trial was performed from the beginning of June to the end of August 2001. To eliminate any effects of animal baseline value, diet sequence, and time, the experiment had a 3 ¥ 3 Latin-square design. There were three different dietary treatments, and the three groups of parrots were randomly allocated to the diet orders. The experimental periods lasted 28 days each. The washout period of the previous treatment occurred during the experimental period. On the last day of each experimental period, blood samples were collected from the jugular vein of each parrot, and the birds were weighed. The blood samples, ranging from about 0.1 to 1.5 mL, were collected in heparinized tubes. Blood was centrifuged (10.000 xg, 10 min), and the plasma samples were stored at –20˚C until further analysis.

Diet Formulation

The experimental diets only differed in fiber source. The control diet contained 6.44% cellulose, on an as-is basis, which was partly or completely exchanged for psyllium on a weight basis to formulate the two experimental diets. The major fat source of the diets was palm kernel oil. The compositions of the experimental diets and their constant components are given in Tables 1 and 2. The composition of the diets was based on a previous study conducted by Bavelaar and Beynen.9 The diets were composed so as to meet the assumed nutrient requirements of parrots15 and were fed as extruded pellets.

Feed Analyses

Dry matter, crude protein, crude fat, crude fiber, and crude ash in the diets were analyzed according to the Weende method. Crude fat was extracted from the feed with chloroform:methanol (2:1, v/v) as described by Folch et al.16 and was subsequently saponified using methanolic sodium hydroxide. The constituent fatty acids were converted into their methyl esters using boron trifluoride in methanol. Fatty acid analyses were performed by gas-liquid chromatography using a flame ionization detector, a Chromopack column (Fused silica, no. 7485, CP.FFAPCB 25 m ¥ 0.32 mm, Chromopack, Middelburg, The Netherlands) and H₂as carrier gas.17 The individual fatty acids are expressed as weight percentage of total methyl esters.

Blood Analyses

Plasma total cholesterol, phospholipids, and triglycerides were determined with commercial test combinations and the Cobas-Bio centrifugal analyzer (Roche Diagnostics, Basel, Switzerland). For the cholesterol and phospholipid determination, Precinorm U (cat. #171743, Boehringer, Mannheim, Germany) was used as the control serum; for the triglyceride determination, Precinorm L (cat. #781827) was used. If more than 150 mL plasma was available, high-density lipoprotein (HDL) cholesterol was determined as soluble cholesterol after precipitation of apo B containing lipoproteins (cat. #543004, Roche, Mannheim, Germany) using the Cobas-Bio autoanalyzer and Precinorm L as the control serum. Low-density lipoprotein (LDL) cholesterol was calculated with the formula of Friedewald et al.18 as LDL cholesterol (mmol/L) = total cholesterol (mmol/L) – triglycerides (mmol/L) / 2.2 – HDL cholesterol (mmol/L). The determination of the cholesterol content of the lipoproteins has been validated for the Bob White quail, but not for the African Grey parrot.

Statistical Analyses

Individual parrots were considered as experimental units. Data were used from 16 birds that had participated in the entire experiment. Plasma lipid values and body weights were subjected to a univariate analysis of variance. The plasma values were logarithmically transformed so that they showed a normal distribution. Group, carry-over effect, dietary treatment, and feeding period were used as fixed factors, and the parrots as a random factor. If a significant (P < .05) effect of one of the fixed factors was observed by analysis of variance, a least significant difference (LSD) test was used to identify statistically significant group differences. The statistical analyses were performed with the computer program SPSS (SPSS Inc, Chicago, IL).

Results

Chemical Analysis of Diets

The results of the diet analyses are given in Table 3. In essence, the diets differed in fiber and carbohydrate content only. Psyllium is recovered in the carbohydrate fraction so that extra psyllium at the expense of cellulose lowered the dietary concentration of crude fiber and raised that of the carbohydrates. The calculated pectin content of the diets was 2.1%.

Feed Consumption and Body Weight

Of the18 parrots, 16 finished the experiment. Two were excluded because of unacceptable weight loss. During the last experimental period, one bird was housed individually in a cage within the aviary because the animal caused fighting; this parrot was not excluded from the experiment.

Before the experiment, the parrots had been fed a commercial diet (Nutribird P15, Versale-Laga, Deinze, Belgium); the mean daily feed intake was 29.5 g per parrot. During the experiment, the mean daily feed intake per bird was 31.4 g for the control diet, 32.8 g for the low-psyllium diet, and 31.0 g for the high-psyllium diet. Because the parrots could not be fed individually, body weight was used as indicator of feed consumption. The experimental diets had no significant influence on body weight (P = .10). Body weights after feeding either the control, low-, or high-psyllium diet were 446 ± 57, 443 ± 57, and 448 ± 57 g (means ± SD, n=16), respectively. The similar body weights for the three diets indicate that the individual parrots consumed equal amounts of energy with each diet and that the dietary variables did not influence palatability. This conclusion is supported by the feed intake values given previously, and the calculated energy contents of the diets (Table 3). Excreta consistency was considered to be normal, irrespective of the type of diet that was fed.

Plasma Analyses

The plasma values for each dietary treatment are given in Table 4. No group and carry-over effects were found. The dietary treatments did not significantly influence any of the plasma lipid concentrations. The feeding periods had a significant influence on plasma phospholipid concentration and on plasma LDL cholesterol concentration. Plasma phospholipids were significantly lower in the first period, and plasma LDL cholesterol concentration was significantly lower in the second period.

Discussion

In studies on the cholesterolemic effect of psyllium, the general approach is to feed a hypercholesterolemic diet as control diet and add psyllium to this diet to formulate the test diet.19 The composition of the control diet used in this study was based on a previous one conducted by Bavelaar and Beynen.9 The results of that study showed that feeding a high-fat diet rich in saturated fatty acids to African Grey parrots results in an increase in plasma cholesterol levels. The composition of the high-fat, hypercholesterolemic diet from that earlier study was almost identical to that of the control diet in the present study. The mean plasma cholesterol level of the parrots fed the control diet was 7.6 mmol/L. Polo et al.20 reported a mean plasma cholesterol level of 6.8 mmol/L for African Greys fed a mixed diet. It appears that the parrots in this study had a high cholesterol level, supporting that the diet fed can be considered hypercholesterolemic.

It is clear from this experiment that dietary psyllium at two inclusion levels had no significant effect on plasma cholesterol concentrations in African Grey parrots. Several explanations for this lack of effect may be put forward. First, African Grey parrots might be insensitive to the hypocholesterolemic effect of psyllium. The statistical power might have been too low to detect an effect of psyllium. The level of psyllium in the diet might have been too low to exert an effect. The type of psyllium might have been inappropriate for an effect on plasma cholesterol to become apparent. The composition of the background composition of the diet, including the pectin content, might have masked any effect of psyllium. Finally, the experimental period might have been too short to alter plasma cholesterol concentrations in the parrots.

The level of plasma cholesterol in African Grey parrots does respond to diet change. Dietary saturated versus polyunsaturated fatty acids have been shown to be hypercholesterolemic in African Grey parrots,9 the same animals used in the present study. Thus, the parrots used can be considered to be responsive to diet composition with regard to plasma cholesterol concentrations. To our knowledge no literature exists on the cholesterolemic effect of psyllium in parrots. However, Fahrenbach et al.12 found that the addition of psyllium to the diet significantly decreased plasma cholesterol concentrations in chickens. The hypocholesterolemic effect of psyllium has also been shown in humans,11,21 rats,10,22 guinea pigs,23,24 hamsters,25,26 rabbits,27 and monkeys.28 It appears that psyllium has a hypocholesterolemic effect in both mammalian and avian species. It is thus difficult to see that the parrots used would be insensitive to psyllium.

Fahrenbach et al.12 found a 29% decrease in plasma cholesterol levels when chickens were fed a diet containing 1.5% (w/w) psyllium and 3% cholesterol (w/w) instead of a diet with cholesterol alone. In hamsters, the addition of 3% psyllium and 0.1% cholesterol to diet decreased plasma cholesterol concentrations by 26% when compared with the addition of cholesterol alone.25 In rats, the addition of 6% psyllium to a diet containing 1% cholesterol decreased plasma cholesterol concentrations by 34% when compared with the cholesterol-containing control diet.22 In this parrot study, either 3.22% or 6.44% psyllium was added to the diet. Based on the literature, it follows that the levels of psyllium used should have been high enough to exert an effect. However, in most experiments, psyllium was added to diets containing cholesterol, which enhances the cholesterolemic effect of psyllium.23,29,30

However, psyllium also had a hypocholesterolemic effect with the use of low-cholesterol or cholesterol-free diets. Fernandez et al.23 found a 32.4% decrease in plasma cholesterol in guinea pigs when 7.5% psyllium was added to the low-cholesterol (0.04%) diet. In hamsters, Horton et al.³⁰ found an 18.3% decrease in plasma cholesterol when the animals were fed a cholesterol-free, low-fat diet and 7.5% psyllium was added. Nevertheless, it is evident that the hypocholesterolemic effect of psyllium is relatively small when the diet used is cholesterol free. The absence of cholesterol in the experimental diets used in this study could in part explain the lack of an effect of psyllium. Cholesterol was not added to the diets because parrots generally do not consume cholesterol-rich diets so that the addition of cholesterol would have decreased the practical relevance of this experiment.

The control diet contained 16.5% fat and 10.8% crude fiber. Commercial parrot diets contain 4% to 22% fat and 2% to 23% crude fiber. The composition of the control diet was within the practical range. As mentioned above, the control diet can be considered hypercholesterolemic and thus was appropriate in this study. However, the pectin content of the diets was 2.1% and this might have masked the cholesterol-lowering effect of psyllium. Pectin has hypocholesterolemic activity11–13 and may exert its action through the same mechanism as does psyllium.25

It is also possible that the statistical power of the present experiment was insufficient. With a group of 16 animals and the observed residual variance of plasma cholesterol concentration, the smallest statistically significant effect (P = .05) is 1.25 mmol/L at a power of 80%. In hamsters, decreases of 2.3231 and 1.51 mmol/L25 have been found when 5% or 3% psyllium was added to cholesterol-containing diets. In rats fed a cholesterol-rich diet with 6% psyllium, a decrease of 1.5 mmol/L was found.22 In another study with parrots, Bavelaar and Beynen⁹ found that a high-fat diet rich in polyunsaturated fatty acids produced a decrease in plasma cholesterol concentrations by about 0.9 mmol/L when compared to a high fat diet rich in saturated fatty acids. Thus, the statistical power to pick up a realistic cholesterolemic effect in this study was not abundant. However, the observed mean plasma cholesterol concentrations were similar for the three dietary treatments. It would follow that any tendency towards a treatment effect was absent and that the marginal statistical power of the study does not weaken interpretation of the outcome.

Another possible explanation for the lack of psyllium effect is that the experimental period was too short. In this experiment, the feeding periods lasted 28 days. Identical periods were used to show the hypocholesterolemic effect of psyllium in hamsters30 and guinea pigs.23,32 Furthermore, in African Grey parrots fed different dietary fats, the effect of diet was seen after 28 days.9 Therefore, it seems likely that the experimental period was sufficiently long to disclose a cholesterolemic effect.

Another matter of interest is the way psyllium was added to the diet. In this study, psyllium was added to the diet mixture before preparation of extruded pellets. During extrusion, the diet ingredients are exposed to high temperature, high pressure, and water. It is possible that under these circumstances, the hypocholesterolemic effect of psyllium was modulated. The psyllium preparation used in this study was also used by Terpstra et al.33 They found a significant decrease in plasma cholesterol concentrations when the psyllium was added to diet of rats. This indicates that the preparation of psyllium used in our study does have hypocholesterolemic properties. Keys et al.34 stated that fibers are more effective when added to the diet in hydrated form instead of as a dry powder. It is feasible that extrusion or the addition of psyllium to the diet mixture in dry form cut its hypocholesterolemic activity.

In conclusion, no cholesterolemic effect of adding either 3.22% or 6.44% psyllium to the diet was found in African Grey parrots. The unexpected lack of effect of psyllium could relate to its physical form in the diet. At this stage, we concluded that dietary inclusion of psyllium is not useful for lowering plasma cholesterol concentrations in parrots. However, psyllium might lower plasma cholesterol levels in parrots under conditions other than those in this study.

Acknowledgments

We thank the Dutch Parrot Refuge for their cooperation and the use of their parrots. Furthermore, we are grateful to Hedwig Van der Horst, DVM, for her assistance during the experiment and to Jan Van der Kuilen, Inez Lemmens, and Robert Hovenier for their analytical assistance, Ton Terpstra for his advice, and Eloy Cruz for the extrusion of the diets.

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Table 1. The Ingredient Composition of
the Constant Components in the Experimental Diets

Table 2. The Ingredient Composition of the Experimental Diets

Low High
Control psyllium psyllium

Ingredients(g/kg)

Cellulose 64.4 32.2 —

Psyllium — 32.2 64.4

Constant 935.6 935.6 935.6
components^*

Total 1000.0 1000.0 1000.0

*See Table 1. Cellulose was exchanged for psyllium on a weight basis.

Ingredients (g/kg)

Palm kernel oil 132.00

Corn 114.79

Wheat 103.25

Oats 57.40

Wheat middlings 45.85

Corn glutenmeal 80.27

Egg 40.19

Sugarbeet pulp, dehydrated 109.02

Corn oil 5.77

Soy beans, extracted 80.27

Corn starch 28.64

Wheat germs 22.98

Molasses, cane 5.77

Yeast, dehydrated 17.21

Barley 34.42

Peas 23.51

Rice 1.18

Alfalfa meal, dehydrated 63.06

Premix 1*9.19

Premix 2†11.44

Lime 11.76

Salt 2.03

*Trace-element premix contained per kg: 49.8 g FeSO₄.7H₂O, 12.9 g MnO₂, 17.1 g ZnSO₄.H₂O, 3.9 g CuSO₄.5H₂O, 62.5 mg KI, 37.5 mg Na₂SeO₃.5H₂O, 1.6 g NiSO₄.5H₂O, 0.3 g NaF, 0.2 g CrCl₃.6H₂0, 0.2 g SnCl₂.2H₂O, 25 mg NH₄VO₃and 913.875 g corn starch as carrier

†Vitamin premix contained per kg: 1.6 g vitamin A (500 IU/g), 0.25 g vitamin D₃(500 IU/g)_, 10 g vitamin E (purity 50 %), 0.1 g vitamin K, 25 mg biotin, 0.15 g folic acid, 1.0 g vitamin B₁₂(purity 0.1%), 300 g choline chloride (purity 50%), 0.4 g thiamin, 0.6 g riboflavin, 5.0 g niacin, 0.6 g pyridoxin, 4.4 g (purity 45%) pantothenic acid and 675.875 g corn starch as carrier.

The International Journal of Applied Research in Veterinary Medicine • Vol. 1, No. 2, Spring 2003

Table 3. The Analyzed Composition of the Experimental Diets

Low High

Chemical analysis (g/kg) Control psyllium psyllium

Dry matter 901 902 901

Crude ash 43.3 44.5 45.8

Crude protein 168.3 168.7 168.7

Crude fibre 108.3 82.4 65.0

Crude fat 164.9 167.6 166.9

Carbohydrates* 416.2 438.4 454.8

Gross energy† (MJ/kg) 17.5 18.0 18.3

Fatty acids
(g/100g methyl esters)

Lauric acid (C12:0) 41.9 42.2 42.1

Myristic acid (C14:0) 12.0 12.1 12.0

Palmitic acid (C16:0) 10.9 10.9 10.9

Stearic acid (C18:0) 2.4 2.4 2.4

Oleic acid (C18:1 n-9) 15.6 15.7 15.7

Linoleic acid (C18:2 n-6) 9.2 9.1 9.3

Alpha-linolenic acid (C18:3n-3) 0.6 0.6 0.6
* Calculated as residual fraction

† The gross energy values (MJ/kg) were taken as follows: protein 23.8; fat 39; carbohydrates 17.

Table 4. The Mean Plasma Values of Total Cholesterol, Phospholipids, Triglycerides, High density lipoprotein (HDL) Cholesterol and Low Density Lipoprotein (LDL) Cholesterol, Expressed as mmol/L, for the Different Dietary Treatments

Measure Control Low psyllium High psyllium

n Mean ± SD n Mean ± SD n Mean ± SD

Total cholesterol 16 7.61 ± 1.29 16 7.74 ± 1.40 15 7.43 ± 1.10

Phospholipids 16 4.96 ± 0.64 16 5.10 ± 0.66 15 4.91 ± 0.41

Triglycerides 16 1.06 ± 0.40 16 1.10 ± 0.36 15 1.15 ± 0.39

HDL cholesterol 14 4.50 ± 0.61 12 4.66 ± 0.75 9 4.54 ± 0.52

LDL cholesterol 14 2.84 ± 0.89 12 2.58 ± 1.00 9 2.65 ± 1.01