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British Poultry Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/cbps20
Energy utilisation in germ‐free and conventional chicks fed diets containing sorbose a
a
a
a
M. Furuse , S. I. Yang , N. Niwa , Y. H. Choi & J. Okumura
a
a
Laboratory of Animal Nutrition, School of Agriculture , Nagoya University , Nagoya, 464–01, Japan Published online: 08 Nov 2007.
To cite this article: M. Furuse , S. I. Yang , N. Niwa , Y. H. Choi & J. Okumura (1991) Energy utilisation in germ‐free and conventional chicks fed diets containing sorbose, British Poultry Science, 32:2, 383-390, DOI: 10.1080/00071669108417363 To link to this article: http://dx.doi.org/10.1080/00071669108417363
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/ page/terms-and-conditions
British Poultry Science (1991) 32: 383-390
ENERGY UTILISATION IN GERM-FREE AND CONVENTIONAL CHICKS FED DIETS CONTAINING SORBOSE M. FURUSE*, S. I. YANG, N. NIWA, Y. H. CHOI AND J. OKUMURA Laboratory of Animal Nutrition, School of Agriculture, Nagoya University, Nagoya 464-01, Japan Downloaded by [University of Arizona] at 18:21 04 November 2014
Received for publication 17th July 1990
Abstract 1. In experiment 1, growing conventional (CV) chicks were fed on diets containing graded amounts (0, 100, 200 and 300 g/kg diet) of sorbose from 4 to 14 d. Protein, fat and energy deposition were determined after carcase analysis. The values for growth, food efficiency, metabolisable energy (ME) and fat and energy depositions declined as the dietary sorbose content increased. 2. In experiment 2, the performances of germ-free (GF) and CV chicks fed on diets with (100 g sorbose/kg diet) or without sorbose were investigated. On both diets, body weight gain, food consumption and protein accumulation in GF chicks were significantly higher than those in CV birds. No significant differences were observed between the dietary treatment except for ME values, which were significantly lower for the sorbose diet. 3. It is suggested that dietary sorbose decreased energy utilisation, and that the microbial contribution to the utilisation of dietary sorbose was negligible in the chicken. INTRODUCTION
Sorbose is a very sweet reducing 2-ketohexose, differing from fructose in terms of its configuration at C-3 and C-4. It occurs naturally in the berries of the mountain ash, Sorbus aucuparia (family Rosaceae), and can be produced by fermentation of sorbitol with Acetobacter suboxydans and also by non-enzymatic condensation of glyceraldehyde and dihydroxy acetone. Dietary sorbose has been shown, in a dose dependent manner, to lower food intake, body fat content, and energy utilisation in growing rats (Furuse et al., 1989) and to decrease very low density lipoprotein (VLDL) concentrations in the serum of growing pigs (Furuse et al., 1990b). Furuse et al. (1990a) have also reported that dietary sorbose decreased liver and abdominal fat contents in laying hens. Serum triglycéride, total cholesterol, low density lipoprotein * To whom all correspondence should be addressed. 383
384
M. FURUSE, S. I. YANG, N. NIWA, Y. H. CHOI AND J. OKUMURA
(LDL), VLDL and chylomicron concentrations also decreased when the diet contained 100 g sorbose/kg. In broilers, abdominal and pectoral-muscle fat contents decreased as the dietary sorbose concentration increased (Furuse et al., 1991). However, neither the influence of dietary sorbose on the energy metabolism of birds nor the contribution of the gut microflora to the metabolism of dietary sorbose have been investigated. Therefore, the effect of graded concentrations of dietary sorbose on the utilisation of energy by growing conventional (CV) chicks was investigated (experiment 1) and the influence of dietary sorbose on the performance of germ-free (GF) and CV chicks was compared (experiment 2).
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MATERIALS AND METHODS
Chicks
Experiment 1. One-day-old Single Comb White Leghorn male chicks were fed on a commercial mash (Marubeni Shiryo Co., Ltd., Tokyo, Japan) for 4 d. Thereafter, the chicks were individually weighed after starving for 3 h and distributed selectively to 5 groups of 5 chicks each, such that mean body weights were as uniform as possible. At this stage, the chicks were housed individually in stainless-steel metabolism cages under continuous lighting in a temperature-controlled room at 30°C. Four of the 5 groups of 5 chicks were given the experimental diets from days 4 to 14 and the 5 chicks in the fifth group were killed by cervical dislocation on day 4 to determine their initial body composition. On the final day of the experiment, all remaining chicks were killed by cervical dislocation and stored at — 20°C to await carcase analysis. Experiment 2. Single Comb White Leghorn chicks of mixed sex, the parents of which were from Gifu Prefectural Poultry Breeding Station in Japan and kept in our poultry house, were used. The details for producing GF birds have been described elsewhere (Yokota et al., 1984). CV chicks were obtained in a CV environment from the same batch of GF eggs. Both types of chick received no food for 2 d after hatching, when they were fed on an adequate diet ad libitum for 4 d. At 6 d of age the GF chicks were reared individually in wire-mesh metabolism cages inside the isolator. The CV controls were reared in the same manner as their GF counterparts. Lighting and temperature in the experimental room were similar to those in experiment 1. At this stage, 5 chicks from each environment were killed to determine body composition. GF and CV chicks were fed on the experimental diets ad libitum for the following 10 d. After the feeding trial, all chicks from both environments were killed and stored as described for experiment 1. Diets
The composition of the control diets used in both experiments is shown in Table 1. Sorbose was added to the control diet at concentrations of 100, 200, and 300 g/kg at the expense of maize starch (experiment 1). In experiment 2,
GERM-FREE CHICKS AND SORBOSE
385
sorbose was mixed into the control diet at the expense of maize starch at 100 g/kg diet. Diets were fortified with vitamins in order to compensate for possible losses during the irradiation procedure for food sterilisation with 60Co irradiation (Coates et al., 1969). TABLE 1
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Composition of the control diets (g/kg)
Ingredients Maize starch Vitamin mixture1 Soya-bean protein isolate Maize oil Mineral mixture1 Choline chloride Inositol L-Methionine Glycine L-Threonine Cellulose 1
Experiment Number 1 2 500-0 494-0 2-0 8-0 226-0 55-0 58-5 1-5 1-0 2-9 4-2 1-2
100-0
Furuse and Okumura (1989).
Experimental procedure
The frozen carcases were minced using a meat grinder. The mince was refrozen in liquid nitrogen, minced for a second time and dried at 55°C for 48 h and finely ground for analysis. The nitrogen contents of carcases, diets, and droppings were determined by the Kjeldahl procedure. The protein content was defined as nitrogen X 6-25. Carcase fat was extracted with diethyl ether using a Soxhlet apparatus and determined gravimetrically. Values of 39*12 kj/g for fat and 23-68 kj/g for protein were used to estimate the energy content of the chick (Fraps, 1946). Protein, fat and energy retentions over the experimental period were estimated by subtracting the initial from final body compositions. The body weight gain, food consumption and food efficiency were obtained over the last 3 d of the experimental period in experiment 2, because spillage was reduced to as little as possible during this period. Droppings were collected during the last 3 d to determine the nitrogen-corrected metabolisable energy (MEN) values of the diets (Hill and Anderson, 1958). An automated bomb colarimeter (Shimadzu CA-4, Shimadzu Co., Kyoto, Japan) was used to determine the gross energy contents of diets and droppings. Statistical analysis
Data were subjected to analysis of variance and the significance of the differences between means was assessed by Duncan's multiple range test (experiment 1). Regression equations were also fitted to the data and are given
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M. FURUSE, S. I. YANG, N. NIWA, Y. H. CHOI AND J. OKUMURA
in the Tables when significant effects were detected. In experiment 2, two-way analysis of variance was performed. RESULTS
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The values for the body weight gain, food consumption, food efficiency, and body composition of chicks fed on the diets containing graded concentrations of sorbose are shown in Table 2. Body weight gain, food efficiency and body fat content decreased linearly as dietary sorbose increased. There was no significant differences in food consumption and body protein content, although a significant linear relationship was obtained between dietary and sorbose content and food intake. TABLE 2
Body weight gain, food consumption, food efficiency, and body composition of chicks fed on diets containing various concentrations of sorbose
Dietary sorbose (g/kg) 0
Body weight gain (g/d) Food consumption (g/d) Food efficiency Body fat content (g/kg) Body protein content (g/kg)
Body weight gain Food consumption Food efficiency Body fat content
6-9» 14-3 0-481» 72» 170
Regression equation 7-18-0-009X* 14-9-0-010X 0-488-0-00038X 76-0-0.143X
100 6-5» 14-2 0-457a 68a 173
200
5-7» 13-7 0-417ab 48b 172
Standard Intercept 0-37 0-71 0-018 3-2
Pooled SEM
300 b
4-l 11-2 0-367b 30' 166
error Slope 0-0020 0-0038 0-000097 0-017
R2 value 0-542 0-279 0-461 0-794
0-45 0-84 0-023 3-6 3-4
P value 0-001 0-05 0-001 0-0001
Means not sharing a common superscript letter are significantly different at P< 0-05. Food efficiency = body weight gain/food intake. *X = sorbose in g.
Fat and protein retentions and energy utilisation of chicks fed on the diets containing the graded amounts of sorbose is shown in Table 3. Fat, protein and energy retentions decreased linearly as the dietary sorbose increased. Dietary sorbose lowered MEN value, MEN intake and efficiency of energy utilisation, although heat loss was not changed by any of the treatments. Body weight gain, food consumption, food efficiency and body composition in GF and CV chicks fed on diets with or without sorbose are given in Table 4. Body weight gain and food consumption were significantly higher in GF than CV birds, although significant dietary effects were not detected. No significant differences in food efficiency and body fat and protein contents were observed in both environmental and dietary treatments. No significant interactions between diets and environments were detected (Table 4). Fat, protein and energy retentions and ME values in the GF and CV chicks fed on the diets with or without sorbose are given in Table 5. Fat and total
387
GERM-FREE CHICKS AND SORBOSE TABLE 3
Fat and protein retentions and energy utilisation of chicks fed on diets containing various concentrations of sorbose Dietary sorbose (g/kg) 0 Fat retained (g/d) Protein retained (g/d) Total energy retained (kj/d) Metabolisable energy (ME, kj/g) ME intake (kj/d) Heat loss (kj/d) EEU 1
0-48 a 1 -30a 49a 12-6a 180 a 131 0-27 a
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Regression equation Fat retained Protein retained Total energy retained ME ME intake EEU
0-53-0-0021X* 0-14-0-0017X 53-0-0-12X 12-6-0-0035X 186-0-16X 0-295-0-00059X
100
200
300
Pooled SEM
0-39a l-27 a 45 a 121" 172 a 127 0-26 a
0-13" 1-11» 31b 12-01' 164» 133 0-191'
-0-12' 0-79" 14' 11-4C 128 b 114 0-10'
0-05 0-09 3-52 0-11 10-2 7-5 0-015
Standard error Intercept Slope 0-044 0-080 3-1 0-098 8-6 0-015
0-0002 0-0004 0-017 0-0005 0-046 0-000079
value
P value
0-813 0-461 0-746 0-714 0-416 0-758
0-0001 0-001 0-0001 0-0001 0-01 0-0001
Means not sharing a common superscript letter are significantly different at P < 0 - 0 5 . Heat loss = ME intake — total energy retained. 1 EEU = Efficiency of energy utilisation (total energy retained/ME intake). *X = sorbose in g.
TABLE 4
Body weight gain, food consumption, food efficiency and body composition in germ-free (GF) and conventional (CV) chicks fed on a control or a sorbose-containing diet Diet Body weight gain (g/d) Food consumption (g/d) Food efficiency
Body fat content
(gAg) Body protein content
(gAg)
Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM
GF 6-8 5-8 6-3a 16-3 15-6 15-9a 0-417 0-368 0-399 58 51 54 167 166 167
CV 4-5 5-0 4-8" 0-61 11-8 12-4 12-1" 0-68 0-355 0-403 0-379 0-036 54 46 50 3-9 170 167 168 2-5
Mean 5-6 5-4
14-1 14-0
0-386 0-386
56 49
169 167
Means not sharing a common superscript letter are significantly different at P < 0-05.
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M. FURUSE, S. I. YANG, N. NIWA, Y. H. CHOI AND J. OKUMURA
energy retention were influenced neither by environmental nor dietary factors. Protein retention was significantly higher in GF than CV birds. Dietary ME value was significantly lowered by sorbose, although the gut microflora did not affect the ME values of diets. There were no significant interactions between diets and environments (Table 5). TABLE 5
Fat, protein and energy retentions and rnetabolisable energy value in germ-free (GF) and conventional (CV) chicks fed on a control or a sorbose-containing diet
Diet
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Fat retained (g/d) Protein retained (g/d) Total energy retained
(HJ/d) Metabolisable energy
(KJ/g)
Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM
GF 0-28 0-20 0-24 1-09 1-05 1-07"
CV 0-26 0-17 0-21 0-05 0-96 0-91 0-93b 0-06
37 33 35
33 28 30
11-3 10-7 11-0
3-17 11-5 10-8 11-1 0-16
Mean 0-27 0-18 1-03 0-98 35
30 11-4» 10-8b
Means not sharing a common superscript letter are significantly different at P < 0-05.
DISCUSSION
It has been reported that dietary sorbose reduced the food intake and body weight gain of growing rats (Furuse et al., 1989). Lowered body weight and depressed food intake were also observed in broilers (Furuse et al., 1991) and laying hens (Furuse et al., 1990a) given dietary sorbose. The results in experiment 1 are in good agreement with these reports. The ME values of the diets decreased as the dietary sorbose content increased. Decreased intake and lowered ME values of diets are associated with a reduction in ME intake. Consequently, fat deposition and energy accumulation were lower in birds fed on diets containing sorbose. These reductions could not be explained by lowered ME intake alone, because the efficiency of energy utilisation also decreased. The ME value of sorbose itself was calculated from the equation relating metabolisability of dietary gross energy to the proportion of sorbose (X) in the diet, as follows: Metabolisability = 0-765(SE 0-00594) - 0-213(SE 0-0318)X (R2 = 0-71, P< 0-0001), where R2 (multiple coefficient of determination) equals the sum of squares of treatments/the sum of squares of total. Thereafter, the following equation,
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GERM-FREE CHICKS AND SORBOSE
389
relating ME (kj/g) to the proportion of sorbose (X), was calculated by multiplying by the gross energy of the control diet (16-4 kj/g): ME = 12-6(SE 0-097) - 3-5(SE 0-52)X (R2 = 0-71, P< 0-0001). It is also possible to derive a value for the ME of sorbose using a published value, 15-3 kj/g (Scott et al., 1982), for the ME for the maize starch which was replaced by sorbose. Using this approach the ME value of sorbose was 11-8 (15-3 — 3-5) kj/g, rather lower and less than 80% of those of glucose or sucrose (15-2 and 15-9 kj/g respectively; Hill, 1969). The reason for the low ME value of sorbose can be explained in terms of its low rate of absorption. Sorbose is known to be absorbed passively and its absorption rate is considerably lower than that of glucose (Bogner and Haines, 1961). Therefore, the gut microflora might be expected to contribute to the utilisation of dietary sorbose and this aspect was investigated using GF and CV chicks in experiment 2. The better growth of GF chicks was in good agreement with that found previously (Furuse and Yokota, 1984b, 1985; Furuse et al, 1985a,b). Significant effects of dietary sorbose were not detected except for the ME values which were lower in the diets containing sorbose, as observed in experiment 1. Enhanced ME value of diets as a result of the presence of the gut microflora has been reported (Furuse and Yokota, 1984a,b; 1985; Furuse et al., 1985a,b), but in the present study no significant difference in ME values was observed between the GF and CV environments. This could be explained, partly but not entirely, by the dietary carbohydrate sources, because Furuse et al. (1985b) reported that a difference in the ME value of diets between GF and CV birds could not be detected when birds were given diets containing maize starch as the sole carbohydrate source. In the present study, the control diet contained maize starch as the only source of carbohydrate. In any event, the difference in ME value was not widened by the inclusion of dietary sorbose. This implies that the microbial contribution to dietary sorbose utilisation was small in chicks. Cezerkawski and Breckenridge (1969) reported that sorbose was fermented very slowly by rumen microbes. Moreover, transit time of diets in the chicken is very short compared to that in other animals. In conclusion, dietary sorbose was abosrbed to a certain extent, but the contribution of the gut microflora to the utilisation of unabsorbed sorbose was small in chicks. ACKNOWLEDGEMENT
L-sorbose was donated by Feed Research Group, Foods Division, Asahi Chemical Industry Co. Ltd., Fuji 416, Japan.
BOGNER,
P.H. & HAINES,
REFERENCES I.A. (1961) Development of intestinal selective absorption of glucose in
newly-hatched chicks. Proceedings of the Society for Experimental Biology and Medicine, 107:
265-267.
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COATES, M.E., FORD, J.E., GREGORY, M.E. & THOMPSON, S.Y. (1969) Effects of gamma-irradiation
on the vitamin content of diets for laboratory animals. Laboratory Animals, 3: 39-49. CZERKAWSKI, J.W. & BRECKENRIDGE, G. (1969) Fermentation of various soluble carbohydrates by rumen-organisms with particular reference to methane production. British Journal of Nutrition, 23: 925-937. FRAPS, G.S. (1946) Composition and productive energy of poultry feeds and rations. Texas Agricultural Experimental Station Bulletin, 678: 4-37. FURUSE, M., ISHII, T., MIYAGAWA, S., NAKAGAWA, J., SHIMIZU, T., WATANABE, T. & OKUMURA, J.
(1991) Effect of dietary sorbose on lipid metabolism in male and female broilers. Poultry Science, 70: 95-102. FURUSE, M., NAKAJIMA, S., NAKAGAWA, J., SHIMIZU, T. & OKUMURA, J. (1990a) Regulation of lipid
metabolism by dietary sorbose in laying hens. Poultry Science, 69: 1508-1512. FURUSE, M. & OKUMURA, J. (1989) Effect of dietary acetic acid levels on protein and energy utilisation in chicks. Poultry Science, 68: 795-798.
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FURUSE, M., TAGISHI, T., NARITA, H., SHIMIZU, T. & OKUMURA, J. (1990b) Effect of dietary sorbose
on lipid metabolism in growing pigs. Japanese Journal of Zootechnical Science, 61: 371-374. FURUSE, M., TAMURA, Y., MATSUDA, S., SHIMIZU, T. & OKUMURA, J. (1989) Lower fat deposition
and energy utilization of growing rats fed diets containing sorbose. Comparative Biochemistry and Physiology, 94A: 813-817. FURUSE, M. & YOKOTA, H. (1984a) Protein and energy utilization in germ-free and conventional chicks given diets containing different levels of dietary protein. British Journal of Nutrition, 51: 255-264. FURUSE, M. & YOKOTA, H. (1984b) The effect of the gut microflora on the growth of chicks fed diets high or marginally adequate in energy. Nutrition Report International, 29: 1293-1300. FURUSE, M. & YOKOTA, H. (1985) Effect of the gut microflora on chick growth and utilisation of protein and energy at different concentrations of dietary protein. British Poultry Science, 26: 97-104. FURUSE, M., YOKOTA, H. & TASAKI, I. (1985a) Influence of energy intake on growth and utilisation of dietary protein and energy in germ-free and conventional chicks. British Poultry Science, 26: 389-397. FURUSE, M., YOKOTA, H. & TASAKI, I. (1985b) Effect of the gut microflora on protein and energy utilization in chicks fed diets containing starch or glucose as a sole dietary carbohydrate source. Japanese Journal of Zootechnical Science, 56: 32-40. HILL, F.W. (1969) Poultry nutrition and nutrient requirements, in: D. CUTHBERTSON (Ed.) Nutrition of Animals of Agricultural Importance. Part 2. Assessment of and factors affecting requirements of farm livestock, pp. 1137-1179 (London, Pergamon Press). HILL, F.W. & ANDERSON, D.L. (1958) Comparison of metabolizable energy and productive energy determinations with growing chicks. Journal of Nutrition, 64: 587-603. SCOTT, M.L., NESHEIM, M.C. & YOUNG, R.J. (1982) Nutrition of the chicken. 3rd Ed. (Ithaca,
M. L. Scott and Associates). YOKOTA, H., FURUSE, OKUMURA, J. & TASAKI, I. (1984) A simple method for production and
rearing of the germ-free chick. Japanese Journal of Zootechnical Science, 55: 600-603.
British Poultry Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/cbps20
Energy utilisation in germ‐free and conventional chicks fed diets containing sorbose a
a
a
a
M. Furuse , S. I. Yang , N. Niwa , Y. H. Choi & J. Okumura
a
a
Laboratory of Animal Nutrition, School of Agriculture , Nagoya University , Nagoya, 464–01, Japan Published online: 08 Nov 2007.
To cite this article: M. Furuse , S. I. Yang , N. Niwa , Y. H. Choi & J. Okumura (1991) Energy utilisation in germ‐free and conventional chicks fed diets containing sorbose, British Poultry Science, 32:2, 383-390, DOI: 10.1080/00071669108417363 To link to this article: http://dx.doi.org/10.1080/00071669108417363
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/ page/terms-and-conditions
British Poultry Science (1991) 32: 383-390
ENERGY UTILISATION IN GERM-FREE AND CONVENTIONAL CHICKS FED DIETS CONTAINING SORBOSE M. FURUSE*, S. I. YANG, N. NIWA, Y. H. CHOI AND J. OKUMURA Laboratory of Animal Nutrition, School of Agriculture, Nagoya University, Nagoya 464-01, Japan Downloaded by [University of Arizona] at 18:21 04 November 2014
Received for publication 17th July 1990
Abstract 1. In experiment 1, growing conventional (CV) chicks were fed on diets containing graded amounts (0, 100, 200 and 300 g/kg diet) of sorbose from 4 to 14 d. Protein, fat and energy deposition were determined after carcase analysis. The values for growth, food efficiency, metabolisable energy (ME) and fat and energy depositions declined as the dietary sorbose content increased. 2. In experiment 2, the performances of germ-free (GF) and CV chicks fed on diets with (100 g sorbose/kg diet) or without sorbose were investigated. On both diets, body weight gain, food consumption and protein accumulation in GF chicks were significantly higher than those in CV birds. No significant differences were observed between the dietary treatment except for ME values, which were significantly lower for the sorbose diet. 3. It is suggested that dietary sorbose decreased energy utilisation, and that the microbial contribution to the utilisation of dietary sorbose was negligible in the chicken. INTRODUCTION
Sorbose is a very sweet reducing 2-ketohexose, differing from fructose in terms of its configuration at C-3 and C-4. It occurs naturally in the berries of the mountain ash, Sorbus aucuparia (family Rosaceae), and can be produced by fermentation of sorbitol with Acetobacter suboxydans and also by non-enzymatic condensation of glyceraldehyde and dihydroxy acetone. Dietary sorbose has been shown, in a dose dependent manner, to lower food intake, body fat content, and energy utilisation in growing rats (Furuse et al., 1989) and to decrease very low density lipoprotein (VLDL) concentrations in the serum of growing pigs (Furuse et al., 1990b). Furuse et al. (1990a) have also reported that dietary sorbose decreased liver and abdominal fat contents in laying hens. Serum triglycéride, total cholesterol, low density lipoprotein * To whom all correspondence should be addressed. 383
384
M. FURUSE, S. I. YANG, N. NIWA, Y. H. CHOI AND J. OKUMURA
(LDL), VLDL and chylomicron concentrations also decreased when the diet contained 100 g sorbose/kg. In broilers, abdominal and pectoral-muscle fat contents decreased as the dietary sorbose concentration increased (Furuse et al., 1991). However, neither the influence of dietary sorbose on the energy metabolism of birds nor the contribution of the gut microflora to the metabolism of dietary sorbose have been investigated. Therefore, the effect of graded concentrations of dietary sorbose on the utilisation of energy by growing conventional (CV) chicks was investigated (experiment 1) and the influence of dietary sorbose on the performance of germ-free (GF) and CV chicks was compared (experiment 2).
Downloaded by [University of Arizona] at 18:21 04 November 2014
MATERIALS AND METHODS
Chicks
Experiment 1. One-day-old Single Comb White Leghorn male chicks were fed on a commercial mash (Marubeni Shiryo Co., Ltd., Tokyo, Japan) for 4 d. Thereafter, the chicks were individually weighed after starving for 3 h and distributed selectively to 5 groups of 5 chicks each, such that mean body weights were as uniform as possible. At this stage, the chicks were housed individually in stainless-steel metabolism cages under continuous lighting in a temperature-controlled room at 30°C. Four of the 5 groups of 5 chicks were given the experimental diets from days 4 to 14 and the 5 chicks in the fifth group were killed by cervical dislocation on day 4 to determine their initial body composition. On the final day of the experiment, all remaining chicks were killed by cervical dislocation and stored at — 20°C to await carcase analysis. Experiment 2. Single Comb White Leghorn chicks of mixed sex, the parents of which were from Gifu Prefectural Poultry Breeding Station in Japan and kept in our poultry house, were used. The details for producing GF birds have been described elsewhere (Yokota et al., 1984). CV chicks were obtained in a CV environment from the same batch of GF eggs. Both types of chick received no food for 2 d after hatching, when they were fed on an adequate diet ad libitum for 4 d. At 6 d of age the GF chicks were reared individually in wire-mesh metabolism cages inside the isolator. The CV controls were reared in the same manner as their GF counterparts. Lighting and temperature in the experimental room were similar to those in experiment 1. At this stage, 5 chicks from each environment were killed to determine body composition. GF and CV chicks were fed on the experimental diets ad libitum for the following 10 d. After the feeding trial, all chicks from both environments were killed and stored as described for experiment 1. Diets
The composition of the control diets used in both experiments is shown in Table 1. Sorbose was added to the control diet at concentrations of 100, 200, and 300 g/kg at the expense of maize starch (experiment 1). In experiment 2,
GERM-FREE CHICKS AND SORBOSE
385
sorbose was mixed into the control diet at the expense of maize starch at 100 g/kg diet. Diets were fortified with vitamins in order to compensate for possible losses during the irradiation procedure for food sterilisation with 60Co irradiation (Coates et al., 1969). TABLE 1
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Composition of the control diets (g/kg)
Ingredients Maize starch Vitamin mixture1 Soya-bean protein isolate Maize oil Mineral mixture1 Choline chloride Inositol L-Methionine Glycine L-Threonine Cellulose 1
Experiment Number 1 2 500-0 494-0 2-0 8-0 226-0 55-0 58-5 1-5 1-0 2-9 4-2 1-2
100-0
Furuse and Okumura (1989).
Experimental procedure
The frozen carcases were minced using a meat grinder. The mince was refrozen in liquid nitrogen, minced for a second time and dried at 55°C for 48 h and finely ground for analysis. The nitrogen contents of carcases, diets, and droppings were determined by the Kjeldahl procedure. The protein content was defined as nitrogen X 6-25. Carcase fat was extracted with diethyl ether using a Soxhlet apparatus and determined gravimetrically. Values of 39*12 kj/g for fat and 23-68 kj/g for protein were used to estimate the energy content of the chick (Fraps, 1946). Protein, fat and energy retentions over the experimental period were estimated by subtracting the initial from final body compositions. The body weight gain, food consumption and food efficiency were obtained over the last 3 d of the experimental period in experiment 2, because spillage was reduced to as little as possible during this period. Droppings were collected during the last 3 d to determine the nitrogen-corrected metabolisable energy (MEN) values of the diets (Hill and Anderson, 1958). An automated bomb colarimeter (Shimadzu CA-4, Shimadzu Co., Kyoto, Japan) was used to determine the gross energy contents of diets and droppings. Statistical analysis
Data were subjected to analysis of variance and the significance of the differences between means was assessed by Duncan's multiple range test (experiment 1). Regression equations were also fitted to the data and are given
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M. FURUSE, S. I. YANG, N. NIWA, Y. H. CHOI AND J. OKUMURA
in the Tables when significant effects were detected. In experiment 2, two-way analysis of variance was performed. RESULTS
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The values for the body weight gain, food consumption, food efficiency, and body composition of chicks fed on the diets containing graded concentrations of sorbose are shown in Table 2. Body weight gain, food efficiency and body fat content decreased linearly as dietary sorbose increased. There was no significant differences in food consumption and body protein content, although a significant linear relationship was obtained between dietary and sorbose content and food intake. TABLE 2
Body weight gain, food consumption, food efficiency, and body composition of chicks fed on diets containing various concentrations of sorbose
Dietary sorbose (g/kg) 0
Body weight gain (g/d) Food consumption (g/d) Food efficiency Body fat content (g/kg) Body protein content (g/kg)
Body weight gain Food consumption Food efficiency Body fat content
6-9» 14-3 0-481» 72» 170
Regression equation 7-18-0-009X* 14-9-0-010X 0-488-0-00038X 76-0-0.143X
100 6-5» 14-2 0-457a 68a 173
200
5-7» 13-7 0-417ab 48b 172
Standard Intercept 0-37 0-71 0-018 3-2
Pooled SEM
300 b
4-l 11-2 0-367b 30' 166
error Slope 0-0020 0-0038 0-000097 0-017
R2 value 0-542 0-279 0-461 0-794
0-45 0-84 0-023 3-6 3-4
P value 0-001 0-05 0-001 0-0001
Means not sharing a common superscript letter are significantly different at P< 0-05. Food efficiency = body weight gain/food intake. *X = sorbose in g.
Fat and protein retentions and energy utilisation of chicks fed on the diets containing the graded amounts of sorbose is shown in Table 3. Fat, protein and energy retentions decreased linearly as the dietary sorbose increased. Dietary sorbose lowered MEN value, MEN intake and efficiency of energy utilisation, although heat loss was not changed by any of the treatments. Body weight gain, food consumption, food efficiency and body composition in GF and CV chicks fed on diets with or without sorbose are given in Table 4. Body weight gain and food consumption were significantly higher in GF than CV birds, although significant dietary effects were not detected. No significant differences in food efficiency and body fat and protein contents were observed in both environmental and dietary treatments. No significant interactions between diets and environments were detected (Table 4). Fat, protein and energy retentions and ME values in the GF and CV chicks fed on the diets with or without sorbose are given in Table 5. Fat and total
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GERM-FREE CHICKS AND SORBOSE TABLE 3
Fat and protein retentions and energy utilisation of chicks fed on diets containing various concentrations of sorbose Dietary sorbose (g/kg) 0 Fat retained (g/d) Protein retained (g/d) Total energy retained (kj/d) Metabolisable energy (ME, kj/g) ME intake (kj/d) Heat loss (kj/d) EEU 1
0-48 a 1 -30a 49a 12-6a 180 a 131 0-27 a
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Regression equation Fat retained Protein retained Total energy retained ME ME intake EEU
0-53-0-0021X* 0-14-0-0017X 53-0-0-12X 12-6-0-0035X 186-0-16X 0-295-0-00059X
100
200
300
Pooled SEM
0-39a l-27 a 45 a 121" 172 a 127 0-26 a
0-13" 1-11» 31b 12-01' 164» 133 0-191'
-0-12' 0-79" 14' 11-4C 128 b 114 0-10'
0-05 0-09 3-52 0-11 10-2 7-5 0-015
Standard error Intercept Slope 0-044 0-080 3-1 0-098 8-6 0-015
0-0002 0-0004 0-017 0-0005 0-046 0-000079
value
P value
0-813 0-461 0-746 0-714 0-416 0-758
0-0001 0-001 0-0001 0-0001 0-01 0-0001
Means not sharing a common superscript letter are significantly different at P < 0 - 0 5 . Heat loss = ME intake — total energy retained. 1 EEU = Efficiency of energy utilisation (total energy retained/ME intake). *X = sorbose in g.
TABLE 4
Body weight gain, food consumption, food efficiency and body composition in germ-free (GF) and conventional (CV) chicks fed on a control or a sorbose-containing diet Diet Body weight gain (g/d) Food consumption (g/d) Food efficiency
Body fat content
(gAg) Body protein content
(gAg)
Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM
GF 6-8 5-8 6-3a 16-3 15-6 15-9a 0-417 0-368 0-399 58 51 54 167 166 167
CV 4-5 5-0 4-8" 0-61 11-8 12-4 12-1" 0-68 0-355 0-403 0-379 0-036 54 46 50 3-9 170 167 168 2-5
Mean 5-6 5-4
14-1 14-0
0-386 0-386
56 49
169 167
Means not sharing a common superscript letter are significantly different at P < 0-05.
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M. FURUSE, S. I. YANG, N. NIWA, Y. H. CHOI AND J. OKUMURA
energy retention were influenced neither by environmental nor dietary factors. Protein retention was significantly higher in GF than CV birds. Dietary ME value was significantly lowered by sorbose, although the gut microflora did not affect the ME values of diets. There were no significant interactions between diets and environments (Table 5). TABLE 5
Fat, protein and energy retentions and rnetabolisable energy value in germ-free (GF) and conventional (CV) chicks fed on a control or a sorbose-containing diet
Diet
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Fat retained (g/d) Protein retained (g/d) Total energy retained
(HJ/d) Metabolisable energy
(KJ/g)
Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM Control Sorbose Mean Pooled SEM
GF 0-28 0-20 0-24 1-09 1-05 1-07"
CV 0-26 0-17 0-21 0-05 0-96 0-91 0-93b 0-06
37 33 35
33 28 30
11-3 10-7 11-0
3-17 11-5 10-8 11-1 0-16
Mean 0-27 0-18 1-03 0-98 35
30 11-4» 10-8b
Means not sharing a common superscript letter are significantly different at P < 0-05.
DISCUSSION
It has been reported that dietary sorbose reduced the food intake and body weight gain of growing rats (Furuse et al., 1989). Lowered body weight and depressed food intake were also observed in broilers (Furuse et al., 1991) and laying hens (Furuse et al., 1990a) given dietary sorbose. The results in experiment 1 are in good agreement with these reports. The ME values of the diets decreased as the dietary sorbose content increased. Decreased intake and lowered ME values of diets are associated with a reduction in ME intake. Consequently, fat deposition and energy accumulation were lower in birds fed on diets containing sorbose. These reductions could not be explained by lowered ME intake alone, because the efficiency of energy utilisation also decreased. The ME value of sorbose itself was calculated from the equation relating metabolisability of dietary gross energy to the proportion of sorbose (X) in the diet, as follows: Metabolisability = 0-765(SE 0-00594) - 0-213(SE 0-0318)X (R2 = 0-71, P< 0-0001), where R2 (multiple coefficient of determination) equals the sum of squares of treatments/the sum of squares of total. Thereafter, the following equation,
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GERM-FREE CHICKS AND SORBOSE
389
relating ME (kj/g) to the proportion of sorbose (X), was calculated by multiplying by the gross energy of the control diet (16-4 kj/g): ME = 12-6(SE 0-097) - 3-5(SE 0-52)X (R2 = 0-71, P< 0-0001). It is also possible to derive a value for the ME of sorbose using a published value, 15-3 kj/g (Scott et al., 1982), for the ME for the maize starch which was replaced by sorbose. Using this approach the ME value of sorbose was 11-8 (15-3 — 3-5) kj/g, rather lower and less than 80% of those of glucose or sucrose (15-2 and 15-9 kj/g respectively; Hill, 1969). The reason for the low ME value of sorbose can be explained in terms of its low rate of absorption. Sorbose is known to be absorbed passively and its absorption rate is considerably lower than that of glucose (Bogner and Haines, 1961). Therefore, the gut microflora might be expected to contribute to the utilisation of dietary sorbose and this aspect was investigated using GF and CV chicks in experiment 2. The better growth of GF chicks was in good agreement with that found previously (Furuse and Yokota, 1984b, 1985; Furuse et al, 1985a,b). Significant effects of dietary sorbose were not detected except for the ME values which were lower in the diets containing sorbose, as observed in experiment 1. Enhanced ME value of diets as a result of the presence of the gut microflora has been reported (Furuse and Yokota, 1984a,b; 1985; Furuse et al., 1985a,b), but in the present study no significant difference in ME values was observed between the GF and CV environments. This could be explained, partly but not entirely, by the dietary carbohydrate sources, because Furuse et al. (1985b) reported that a difference in the ME value of diets between GF and CV birds could not be detected when birds were given diets containing maize starch as the sole carbohydrate source. In the present study, the control diet contained maize starch as the only source of carbohydrate. In any event, the difference in ME value was not widened by the inclusion of dietary sorbose. This implies that the microbial contribution to dietary sorbose utilisation was small in chicks. Cezerkawski and Breckenridge (1969) reported that sorbose was fermented very slowly by rumen microbes. Moreover, transit time of diets in the chicken is very short compared to that in other animals. In conclusion, dietary sorbose was abosrbed to a certain extent, but the contribution of the gut microflora to the utilisation of unabsorbed sorbose was small in chicks. ACKNOWLEDGEMENT
L-sorbose was donated by Feed Research Group, Foods Division, Asahi Chemical Industry Co. Ltd., Fuji 416, Japan.
BOGNER,
P.H. & HAINES,
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