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British Poultry Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/cbps20
Effect of short chain fatty acids on the performance and intestinal weight in germ‐free and conventional chicks a
a
a
M. Furuse , S. I. Yang , N. Niwa & 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 & J. Okumura (1991) Effect of short chain fatty acids on the performance and intestinal weight in germ‐free and conventional chicks, British Poultry Science, 32:1, 159-165, DOI: 10.1080/00071669108417337 To link to this article: http://dx.doi.org/10.1080/00071669108417337
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: 159-165
EFFECT OF SHORT CHAIN FATTY ACIDS ON THE PERFORMANCE AND INTESTINAL WEIGHT IN GERM-FREE AND CONVENTIONAL CHICKS M. FURUSE, S. I. YANG, N. NIWA AND J. OKUMURA Laboratory of Animal Nutrition, School of Agriculture, Nagoya University, Nagoya 464-01, Japan
Downloaded by [New York University] at 01:28 16 April 2015
Received for publication 2nd January 1990
Abstract 1. In experiment 1, the performance and tissue weights of germ-free (GF) and conventional (CV) chicks fed on diets containing 25'4 g acetic acid/kg diet (AD) or 25.4 g kaolin/kg diet (KD) were investigated. Body weight gain in GF chicks was significantly higher on the AD, but significantly lower on the KD compared with their CV counterparts. The values for food efficiency, protein retention and energy retention followed a similar pattern to that of the body weight gain. 2. The weights of all sections of the intestine except the colon were significantly greater in CV chicks. In CV but not in GF birds the jejunum and ileum were heavier from birds fed on the AD than from those on the KD diet. 3. In experiment 2, the influence of butyric acid administration on the weight of some organs in chicks was investigated. The weight of duodenum, jejunum and ileum was significantly increased by intraperitoneal administration of butyric acid (2 ml of 100 mM solution/d) for 4 d, but no significant effect was observed by oral administration. 4. It might be suggested that short chain fatty acids such as acetic and butyric acids formed by bacterial action in the crop and subsequently absorbed are at least partly responsible for the heavier gut weight in CV birds. INTRODUCTION
Short chain fatty acids (SCFA) with a chain length ranging from one to six carbon atoms are the major end-products of the microbial digestion of carbohydrates in the digestive tract. In ruminants and non-ruminant herbivores, the metabolic roles of SCFA have been investigated in detail and are known to stimulate epithelial cell division in the digestive tract (Sakata and Yajima, 1984) and to influence the development of the ruminant stomach (Warner and Flatt, 1965). Faster migration rates of epithelial cells of conventional (CV) animals compared with germ-free (GF) counterparts have been reported (Abrams et al., 159
Downloaded by [New York University] at 01:28 16 April 2015
160
M. FURUSE ET AL.
1963; Rolls et al., 1978). Likewise, the GF animal also has lighter and thinner intestines compared to the CV controls (Gordon et al., 1966, Furuse and Yokota, 1984a). The exact reasons for these differences between GF and CV animals are so far unknown. One possible reason is that a certain SCFA produced by the gut microflora might induce the physiological changes in the intestine, because SCFA contents in the digestive tracts of GF animals are low compared to those of CV ones (Annison et al., 1968; Hoverstad and Midtvedt, 1986). Little information is available on the nutritional and physiological role of SCFA in avian species. Recently, Furuse and Okumura (1989) reported that dietary acetic acid affected the performance of growing chicks. Although growth was gradually reduced with increasing dietary acetic acid contents when chicks were fed ad libitum, it was somewhat, but not significantly, improved, by the supplementary acetic acid under equalised-feeding conditions. They used the CV bird in which SCFA should already be present in the digestive tract. Accordingly, the exact role of acetic acid for the host animal has not been investigated. The objectives of the present study were; firstly to determine the effect of dietary acetic acid on the performance as well as on the weight of some tissues of GF chicks and secondly to compare the effect on the organ weight of butyric acid by oral and intraperitoneal administration. MATERIALS AND METHODS
Experiment 1
Chicks. Single comb White Leghorn chicks of mixed sexes were used, the parents of which were from Gifu Prefectural Poultry Breeding Station in Japan and kept in our poultry house. The details for the method of producing GF birds are described elsewhere (Yokota et al., 1984). The chicks received no food for 2 d after hatching, then were fed 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. GF and CV chicks were fed on the experimental diets ad libitum for the following 10 d. Diets. Table 1 shows the composition of the experimental diets. The powdered acetic acid used in the present study was made by mixing acetic acid with dextrin, and was a gift from Nakano Vinegar Co. Ltd., Handa, Japan. Its composition is given in Table 1. Kaolin was present in the control diet in place of dietary acetic acid. The diets were fortified with vitamins in order to compensate for possible losses resulting from the 60Co-irradiation procedure for food sterilisation (Coates et al., 1969). Experimental procedure. At 16 d of age, 5 GF and CV chicks were killed by cervical dislocation. The abdominal cavity was opened and duodenum, jeju-
GERM-FREE CHICKS AND ACETIC ACID
161
TABLE 1
Downloaded by [New York University] at 01:28 16 April 2015
Composition of the experimental diets (g/kg)
Acetic acid (g/kg) Ingredients 0 25-4 Powdered acetic acid (SK-1)1 0 200 Dextrin 174-6 0 Kaolin 25-4 0 Soyabean protein isolate2 226 55 Maize oil 3 Mineral mixture 58-5 8 Vitamin mixture3 1-5 Choline chloride 1 Inositol L-Methionine 2-9 Glycine 4-2 1-2 L-Threonine 100 Cellulose Maize starch up to 1000 1 The SK-1 (Nakano Vinegar Co. Ltd., Handa, Japan) is composed by 127 g/kg acetic acid and 873 g/kg dextrin. 2 Fujipro-R, Fuji Oil Co. Ltd., Osaka, Japan. 3 Muramatsu et al. (1985).
num, ileum, caecum and colon were removed quickly. The intestine was cut longitudinally, and its contents removed by washing with 0-15 M sodium chloride. The intestine was blotted, weighed, frozen by plunging into liquid nitrogen and stored at — 20°C until analysis. The remaining carcase was also frozen using liquid nitrogen. The carcases, including intestine, were minced, frozen again with liquid nitrogen, minced for a second time and then dried at 55°C for 48 h before being finely ground for analysis. The nitrogen content of carcases was determined by the Kjeldahl procedure. The crude protein content was defined as N X 6-25. Carcase fat was determined gravimetrically following Soxhlet extraction. 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). At day 2, five chicks from each environment were killed to determine body composition. Protein, fat and energy retention over the experimental period were estimated by subtracting the initial body composition from the final values. The value for the food efficiency was obtained over the last 3 d of the experimental period. Experiment 2
Chicks. CV single comb White Leghorn male chicks (10-d-old) were fed on a commercial chick mash (Marubeni Shiryo Co. Ltd., Tokyo, Japan). They were divided into three groups of 5 chicks each. The control group was given 2 ml/bird/d of saline (0-15 M sodium chloride) by intraperitoneal injection. The other two groups were given 2 ml/bird/d of 100 mM butyric acid in saline by either oral or intraperitoneal injection. Experimental procedure. Injection was done once a day for 4 d. Twenty four hours after the final administration, chicks were weighted and killed by cervical
162
M. FURUSE ETAL. TABLE 2
Body weight gain, food efficiency and retentions of protein, fat and energy in germ-free (GF) and conventional (CV) chicks fed on diets with (AD) or without (KD) dietary acetic acid
Analysis of variance Body weight gain (g/10 d)
Diet
GF
AD KD
65-4 58-2 54-0 61-8 11-4** -3-6 59-7 60-0 23-3 0-52 0-45 0-37 0-47 0-15*** -0-02 0-44 0-46 0-0035 13-9 12-0 11-1 12-5 2-8*** -0-5 12-5 12-2 1.20 6-15 4-20 4-54 4-53 5.34 4-37 2-40
AD-KD Mean RMS
Food efficiency
AD KD
AD-KD Mean
Downloaded by [New York University] at 01:28 16 April 2015
RMS
Protein retention AD KD (g/10 d) AD-KD Mean RMS
Fat retention (g/10d)
AD KD
Mean RMS
Energy retention (HI/10 d)
AD KD
570 439
AD-KD Mean
131* 505
CV
448 472 24 460
Mean 61-8 57-9
0-48 0-42
130
11-8
5-18 4-54
509 456
GF-CV 7-2* -7-8*
0-07 0-10*
1-9* -1-4
Env X Diet
Env
Diet
NS
NS
NS
*
**
NS
*
**
NS
NS
NS
NS
NS
*
1-95 001
122* -33
6462 Abbreviations: Env, environment; RMS, residual mean square. Significance levels: *P
British Poultry Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/cbps20
Effect of short chain fatty acids on the performance and intestinal weight in germ‐free and conventional chicks a
a
a
M. Furuse , S. I. Yang , N. Niwa & 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 & J. Okumura (1991) Effect of short chain fatty acids on the performance and intestinal weight in germ‐free and conventional chicks, British Poultry Science, 32:1, 159-165, DOI: 10.1080/00071669108417337 To link to this article: http://dx.doi.org/10.1080/00071669108417337
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: 159-165
EFFECT OF SHORT CHAIN FATTY ACIDS ON THE PERFORMANCE AND INTESTINAL WEIGHT IN GERM-FREE AND CONVENTIONAL CHICKS M. FURUSE, S. I. YANG, N. NIWA AND J. OKUMURA Laboratory of Animal Nutrition, School of Agriculture, Nagoya University, Nagoya 464-01, Japan
Downloaded by [New York University] at 01:28 16 April 2015
Received for publication 2nd January 1990
Abstract 1. In experiment 1, the performance and tissue weights of germ-free (GF) and conventional (CV) chicks fed on diets containing 25'4 g acetic acid/kg diet (AD) or 25.4 g kaolin/kg diet (KD) were investigated. Body weight gain in GF chicks was significantly higher on the AD, but significantly lower on the KD compared with their CV counterparts. The values for food efficiency, protein retention and energy retention followed a similar pattern to that of the body weight gain. 2. The weights of all sections of the intestine except the colon were significantly greater in CV chicks. In CV but not in GF birds the jejunum and ileum were heavier from birds fed on the AD than from those on the KD diet. 3. In experiment 2, the influence of butyric acid administration on the weight of some organs in chicks was investigated. The weight of duodenum, jejunum and ileum was significantly increased by intraperitoneal administration of butyric acid (2 ml of 100 mM solution/d) for 4 d, but no significant effect was observed by oral administration. 4. It might be suggested that short chain fatty acids such as acetic and butyric acids formed by bacterial action in the crop and subsequently absorbed are at least partly responsible for the heavier gut weight in CV birds. INTRODUCTION
Short chain fatty acids (SCFA) with a chain length ranging from one to six carbon atoms are the major end-products of the microbial digestion of carbohydrates in the digestive tract. In ruminants and non-ruminant herbivores, the metabolic roles of SCFA have been investigated in detail and are known to stimulate epithelial cell division in the digestive tract (Sakata and Yajima, 1984) and to influence the development of the ruminant stomach (Warner and Flatt, 1965). Faster migration rates of epithelial cells of conventional (CV) animals compared with germ-free (GF) counterparts have been reported (Abrams et al., 159
Downloaded by [New York University] at 01:28 16 April 2015
160
M. FURUSE ET AL.
1963; Rolls et al., 1978). Likewise, the GF animal also has lighter and thinner intestines compared to the CV controls (Gordon et al., 1966, Furuse and Yokota, 1984a). The exact reasons for these differences between GF and CV animals are so far unknown. One possible reason is that a certain SCFA produced by the gut microflora might induce the physiological changes in the intestine, because SCFA contents in the digestive tracts of GF animals are low compared to those of CV ones (Annison et al., 1968; Hoverstad and Midtvedt, 1986). Little information is available on the nutritional and physiological role of SCFA in avian species. Recently, Furuse and Okumura (1989) reported that dietary acetic acid affected the performance of growing chicks. Although growth was gradually reduced with increasing dietary acetic acid contents when chicks were fed ad libitum, it was somewhat, but not significantly, improved, by the supplementary acetic acid under equalised-feeding conditions. They used the CV bird in which SCFA should already be present in the digestive tract. Accordingly, the exact role of acetic acid for the host animal has not been investigated. The objectives of the present study were; firstly to determine the effect of dietary acetic acid on the performance as well as on the weight of some tissues of GF chicks and secondly to compare the effect on the organ weight of butyric acid by oral and intraperitoneal administration. MATERIALS AND METHODS
Experiment 1
Chicks. Single comb White Leghorn chicks of mixed sexes were used, the parents of which were from Gifu Prefectural Poultry Breeding Station in Japan and kept in our poultry house. The details for the method of producing GF birds are described elsewhere (Yokota et al., 1984). The chicks received no food for 2 d after hatching, then were fed 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. GF and CV chicks were fed on the experimental diets ad libitum for the following 10 d. Diets. Table 1 shows the composition of the experimental diets. The powdered acetic acid used in the present study was made by mixing acetic acid with dextrin, and was a gift from Nakano Vinegar Co. Ltd., Handa, Japan. Its composition is given in Table 1. Kaolin was present in the control diet in place of dietary acetic acid. The diets were fortified with vitamins in order to compensate for possible losses resulting from the 60Co-irradiation procedure for food sterilisation (Coates et al., 1969). Experimental procedure. At 16 d of age, 5 GF and CV chicks were killed by cervical dislocation. The abdominal cavity was opened and duodenum, jeju-
GERM-FREE CHICKS AND ACETIC ACID
161
TABLE 1
Downloaded by [New York University] at 01:28 16 April 2015
Composition of the experimental diets (g/kg)
Acetic acid (g/kg) Ingredients 0 25-4 Powdered acetic acid (SK-1)1 0 200 Dextrin 174-6 0 Kaolin 25-4 0 Soyabean protein isolate2 226 55 Maize oil 3 Mineral mixture 58-5 8 Vitamin mixture3 1-5 Choline chloride 1 Inositol L-Methionine 2-9 Glycine 4-2 1-2 L-Threonine 100 Cellulose Maize starch up to 1000 1 The SK-1 (Nakano Vinegar Co. Ltd., Handa, Japan) is composed by 127 g/kg acetic acid and 873 g/kg dextrin. 2 Fujipro-R, Fuji Oil Co. Ltd., Osaka, Japan. 3 Muramatsu et al. (1985).
num, ileum, caecum and colon were removed quickly. The intestine was cut longitudinally, and its contents removed by washing with 0-15 M sodium chloride. The intestine was blotted, weighed, frozen by plunging into liquid nitrogen and stored at — 20°C until analysis. The remaining carcase was also frozen using liquid nitrogen. The carcases, including intestine, were minced, frozen again with liquid nitrogen, minced for a second time and then dried at 55°C for 48 h before being finely ground for analysis. The nitrogen content of carcases was determined by the Kjeldahl procedure. The crude protein content was defined as N X 6-25. Carcase fat was determined gravimetrically following Soxhlet extraction. 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). At day 2, five chicks from each environment were killed to determine body composition. Protein, fat and energy retention over the experimental period were estimated by subtracting the initial body composition from the final values. The value for the food efficiency was obtained over the last 3 d of the experimental period. Experiment 2
Chicks. CV single comb White Leghorn male chicks (10-d-old) were fed on a commercial chick mash (Marubeni Shiryo Co. Ltd., Tokyo, Japan). They were divided into three groups of 5 chicks each. The control group was given 2 ml/bird/d of saline (0-15 M sodium chloride) by intraperitoneal injection. The other two groups were given 2 ml/bird/d of 100 mM butyric acid in saline by either oral or intraperitoneal injection. Experimental procedure. Injection was done once a day for 4 d. Twenty four hours after the final administration, chicks were weighted and killed by cervical
162
M. FURUSE ETAL. TABLE 2
Body weight gain, food efficiency and retentions of protein, fat and energy in germ-free (GF) and conventional (CV) chicks fed on diets with (AD) or without (KD) dietary acetic acid
Analysis of variance Body weight gain (g/10 d)
Diet
GF
AD KD
65-4 58-2 54-0 61-8 11-4** -3-6 59-7 60-0 23-3 0-52 0-45 0-37 0-47 0-15*** -0-02 0-44 0-46 0-0035 13-9 12-0 11-1 12-5 2-8*** -0-5 12-5 12-2 1.20 6-15 4-20 4-54 4-53 5.34 4-37 2-40
AD-KD Mean RMS
Food efficiency
AD KD
AD-KD Mean
Downloaded by [New York University] at 01:28 16 April 2015
RMS
Protein retention AD KD (g/10 d) AD-KD Mean RMS
Fat retention (g/10d)
AD KD
Mean RMS
Energy retention (HI/10 d)
AD KD
570 439
AD-KD Mean
131* 505
CV
448 472 24 460
Mean 61-8 57-9
0-48 0-42
130
11-8
5-18 4-54
509 456
GF-CV 7-2* -7-8*
0-07 0-10*
1-9* -1-4
Env X Diet
Env
Diet
NS
NS
NS
*
**
NS
*
**
NS
NS
NS
NS
NS
*
1-95 001
122* -33
6462 Abbreviations: Env, environment; RMS, residual mean square. Significance levels: *P
