Dietary Pectic Oligosaccharide Administration ... - ACS Publications

The contents of POS and corn starch are 30 and 70% in the product, ..... the level of immunoglobulin in children with rotavirus diarrhea,(11, 12, 28-3...
0 downloads 0 Views 368KB Size
Subscriber access provided by University of Newcastle, Australia

Article

Dietary pectic oligosaccharide administration improves the growth performance and immunity in weaned pigs infected by rotavirus Hao Chen, Haiyan Hu, Daiwen Chen, Jun Tang, BING YU, Junqiu Luo, Jun He, Yuheng Luo, Jie Yu, and Xiangbing Mao J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b00039 • Publication Date (Web): 21 Mar 2017 Downloaded from http://pubs.acs.org on March 25, 2017

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Journal of Agricultural and Food Chemistry is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 31

Journal of Agricultural and Food Chemistry

1

Dietary pectic oligosaccharide administration improves the growth performance

2

and immunity in weaned pigs infected by rotavirus

3 4

Hao Chen†, §, Haiyan Hu†, §, Daiwen Chen†, §, Jun Tang†, §, Bing Yu†, §, Junqiu Luo†, §,

5

Jun He†, §, Yuheng Luo†, §, Jie Yu†, §, Xiangbing Mao†, §, *

6 7



8

Republic of China

9

§

Animal Nutrition Institute, Sichuan Agricultural University, Ya’an, Sichuan, People’s

Key Laboratory of Animal Disease-Resistance Nutrition, Ministry of Education,

10

China, Ya’an, Sichuan, People’s Republic of China

11

*

12

+86-835-2885106, E-mail: [email protected].

Corresponding

author,

Associate Professor

Xiangbing

13

1

ACS Paragon Plus Environment

Mao,

Phone/Fax:

Journal of Agricultural and Food Chemistry

14

ABSTRACT

15

Rotavirus infection is one of the main pathogenic causes of gastroenteritis and

16

diarrhea in children and young animals. The present study aimed to determine

17

whether dietary pectic oligosaccharide (POS) supplementation could improve the

18

growth performance and immunity in weaned pigs infected by porcine rotavirus

19

(PRV). Twenty-eight crossbred weaned galts were randomly divided into two groups

20

fed with basal diet with or without POS for 18 d. On 15th day, the PRV were orally

21

infused to half of the pigs. ADFI, ADG and F/G ratio were impaired by PRV infection

22

in weaned pigs (P < 0.05). PRV challenge also induced diarrhea, and enhanced serum

23

levels of urea nitrogen (P < 0.05), MDA (P < 0.05), IgA (P < 0.05) and IgG (P = 0.08),

24

rotavirus antibody levels in serum, jejunal and ileal mucosa (P < 0.05), IL-2 levels in

25

the jejunal (P = 0.07) and ileal (P = 0.08) mucosa, but decreased digestive enzyme

26

activities of the jejunal digesta (P < 0.05), concentrations of sIgA, IL-4 and IFN-γ in

27

the jejunal and ileal mucosa (P < 0.05), and serum T-AOC (P < 0.05) in the weaned

28

pigs. POS administration could improve the growth performance of the weaned pigs

29

(P < 0.05), and enhance the serum IgA level (P < 0.05), the lipase and tryptase

30

activities of jejunal digesta (P < 0.05), and the sIgA, IL-4 and IFN-γ levels of jejunal

31

and/or ileal mucosa (P < 0.05) in the weaned pigs. Furthermore, supplementing POS

32

in diets could alleviate diarrhea and decreasing growth performance in the weaned

33

pigs orally infused by PRV (P < 0.05), increase serum, jejunal and ileal rotavirus

34

antibody levels (P < 0.05), and attenuate the effect of PRV challenge on serum T-AOC

35

and concentrations of IgG and MDA (P < 0.05), lipase and tryptase activities in

2

ACS Paragon Plus Environment

Page 2 of 31

Page 3 of 31

Journal of Agricultural and Food Chemistry

36

jejunal digesta (P < 0.05), and sIgA, IL-4 and IFN-γ levels in jejunal and/or ileal

37

mucosa (P < 0.05) in the weaned pigs. These results suggest that dietary POS

38

supplementation could improve the growth performance, which was possibly due that

39

POS administration improved the immune function and the utilization of nutrients in

40

the PRV-infection piglets. This offers a potential dietary intervention strategy against

41

intestinal exposure to rotavirus in piglets.

42 43

KEY WORDS: pectic oligosaccharide, rotavirus, immunity, growth performance,

44

weaned pig.

45

3

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

46

Page 4 of 31

INTRODUCTION

47

Because of the lower immune function and uncompleted-development digestive

48

tract, young animals and children are prone to intestinal diseases, such as diarrhea,

49

that will be harmful of growth performance

50

main pathogenic causes of gastroenteritis and diarrhea in children and young animals

51

4, 5

52

intestine health, and induce the inflammatory response in the children and weaned

53

pigs 6-8.

1-3

. Rotavirus (RV) infection is a kind of

. Moreover, some researchers also reported that rotavirus infection could impair the

Many studies have shown that some additives, including the functional

54

8-12

55

oligosaccharide, can decrease the diarrhea that was induced by RV in pigs

.

56

Furthermore, the functional oligosaccharide has many biological virtues, including

57

improving immunity, which is beneficial to the growth of children and young animals

58

13-19

59

the animals from the infection of some viruses and germs 20, 21. As a kind of functional

60

oligosaccharide, pectic oligosaccharide (POS), which is derived from polysaccharides

61

of plant cell wall, also have the similar physiological function in children and animals

62

13, 22

. Furthermore, some oligosaccharide administration can, to some extent, protect

.

63

Therefore, the aim of this study was to verify the hypothesis that supplementing

64

POS in diets might improve growth performance and immune function of the

65

PRV-infection piglets.

66

MATERIALS AND METHODS

67

Animals and diets

4

ACS Paragon Plus Environment

Page 5 of 31

Journal of Agricultural and Food Chemistry

68

The experimental protocol was approved by Animal Care Advisory Committee

69

of Sichuan Agricultural University. Twenty-eight DLY (Duroc × Landrace × Yorkshire)

70

weaned galts (7.54 ± 0.31 kg) were fed in the metabolic cages (1.5 m × 0.7 m × 1.0

71

m). The pigs were fed with the experimental diets 4 times daily at 08.00, 12.00, 16.00

72

and 20.00, and freely drank water. Following 3 d for orientation, these piglets were

73

divided randomly into two groups on basis of body weight and litter origin, and were

74

fed with basal diet (Control group, n = 14) or basal diet with 200 mg/kg apple pectic

75

oligosaccharide product (POS group, n = 14) for 18 d.

76

The basal diet was formulated to meet NRC (2012)

23

nutrient recommendations

77

for pigs (7-11 kg). Its composition and nutrient content were listed in Table 1. The

78

POS group diet was formed via supplementing with 200 mg/kg apple pectic

79

oligosaccharide product in basal diet. The apple pectic oligosaccharide product was

80

obtained from Hebei Kena Biological Technology Co. Ltd. (Hebei, China). The

81

contents of POS and corn starch are 30% and 70% in the product, respectively.

82

POS were produced by pectinase hydrolysis of pectic acid with 26.6% of

83

methylation, which was obtained by chemical hydrolysis of apple pectin. The high

84

performance liquid chromatography (HPLC) detection showed that POS content was

85

more than 55%, and monosaccharide content was more than 20% in the apple pectic

86

oligosaccharide product. Analysis of the electrospray ionization-mass spectrometry

87

(ESI-MS) showed that POS product mainly contain pectic disaccharide, pectic

88

trisaccharide, and a high degree of polymerization of POS.

89

On 15th day, all piglets were infused 5 mL of sterile NaHCO3 solution (100

5

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

90

mmol/L). Then, half of piglets in two groups were orally administrated with 4 mL

91

(106 Tissue culture infective dose 50 (TCID50)/mL) of PRV, and the other piglets

92

were infused with 4 mL of the sterile essential medium. After PRV infusion, the

93

diarrhea status of all piglets was recorded based on Table 2. Pigs were deemed

94

diarrhea when their daily fecal consistency scores is ≥ 2 24. Average daily weight gain

95

(ADG), average daily feed intake (ADFI) and feed/gain ratio (F/G ratio) were

96

calculated via weighing body weight and feed intake of all piglets at 08.00 of d 1, 15

97

and 19.

98

Experimental design and sample collection

99

On 19th day, following weighing, the blood of pigs were gathered through the

100

jugular vein, and isolated serum samples were made by centrifuging blood at 3500 g

101

for 10 min. Then, all piglets were fed with their diets. At 1.5 h after refeeding, all pigs

102

were euthanized via intracardially injecting Na pentobarbital (50 mg/kg of body

103

weight) and exsanguinating. The jejunum and ileum were separated, and rinsed with

104

ice-cold saline. The mucosa of jejunum and ileum was gathered by scraping the gut

105

wall with a glass microscope slide, and frozen in liquid nitrogen. Approximately 3 g

106

of the digesta from the jejunum were collected in sterile tubes, and frozen in liquid

107

nitrogen. Following collection, all samples were stored at -80°C.

108

PRV preparation

109

In the present study, PRV was a tissue culture-adapted Ohio State University

110

(OSU) strain (ATCC #VR-893). The viral propagation, collection and titre

111

determination with IPEC-J2 cells were determined as described previously 25-27.

6

ACS Paragon Plus Environment

Page 6 of 31

Page 7 of 31

Journal of Agricultural and Food Chemistry

112

Analysis of the serum urea nitrogen, serum and intestinal rotavirus antibody and

113

immunoglobulin (Ig) concentrations

114

Serum urea nitrogen (UN) concentration was analyzed with an assay kit (Nanjing

115

Jiancheng Biochemistry, Nanjing, China) on the basis of the manufacturer’s

116

instructions. The rotavirus antibody (RV-Ab) concentrations in serum, jejunal and

117

ileal mucosa were determined with a commercially available pig enzyme-linked

118

immunosorbent assay (ELISA) kit (TSZ ELISA, Framingham, MA) on the basis of

119

the manufacturer’s instructions. IgA, IgG and IgM levels in serum were analyzed with

120

commercially available ELISA kits (Nuoyuan Co. Ltd., Shanghai, China).

121

Analysis of the digestive enzymes activities in the jejunal digesta

122

Before the determination, the samples need to homogenate pretreatment. The

123

0.2-1.0 g of jejunum digesta was added into the homogenate medium (saline)

124

according to the quality of volume ratio 1:9 (g/mL), and executed the ultrasonic

125

pulverization, and then centrifuged at 2000 g for 10 min at 4°C. In the supernatant,

126

the amylase, lipase and tryptase activities were determined by using the ultraviolet

127

spectrophotometer and assay kits (Nanjing Jiancheng Biochemistry, Nanjing, China)

128

on the basis of the manufacturer’s instructions.

129

Analysis of the sIgA and cytokine concentrations in the jejunal and ileal mucosa

130

The 100 mg of the intestinal mucosa was added into the ice-cold PBS, and

131

executed the pulverization at 4°C, and then centrifuged at 5000 g for 15 min at 4°C.

132

In the supernatant, the sIgA, IFN-γ, IL-2 and IL-4 concentrations were determined

133

with commercially available pig ELISA kits (Nuoyuan Co. Ltd., Shanghai, China) on

7

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

134

the basis of the manufacturer’s instructions.

135

Analysis of the serum antioxidant capacity

136

Serum malondialdehyde (MDA) concentration and total antioxidant capacity (T-AOC)

137

were analyzed with assay kits (Nanjing Jiancheng Biochemistry, Nanjing, China) on

138

the basis of the manufacturer’s instructions.

139

Statistical analysis

140

The growth performance data of all piglets before PRV challenge were analyzed

141

with the unpaired t test. The other data were analyzed as a 2 × 2 factorial with the

142

general linear model procedures of the Statistical Analysis Package. The model

143

factors included the effects of POS administration (with or without POS in diets),

144

PRV infection (PRV unchallenged or challenged), and their interaction. All data were

145

analyzed with SAS (Version8.1; SAS Institute, Gary, NC). All data were indicated as

146

means with their standard errors. P value less than 0.05 was considered statistical

147

significance while P value less than 0.10 was considered statistical tendency.

148

RESULTS

149

Growth performance of weaned pigs

150

During the experiment, there were not any unexpected deaths. During the trial,

151

supplementing POS in the diet increased ADG and reduced F/G ratio of pigs between

152

1-14 days (P < 0.05) (Table 3). However, PRV infusion reduced ADFI and ADG and

153

increased F/G ratio of weaned pigs (P < 0.05). But dietary POS supplementation

154

relieved the effect of PRV infection on ADFI, ADG and F/G ratio of weaned pigs (P