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Effects of Forsythia Suspense Extract as an Antibiotics Substitute on Growth Performance, Nutrient Digestibility, Serum Antioxidant Capacity, Fecal Escherichia coli Concentration and Intestinal Morphology of Weaned Piglets

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Simple Summary: Weaning stress may reduce feed intake, weight gain and health status of piglets. Antibiotics are used to overcome post-weaning disorders. However, the abuse of antibiotics in pig feed has become a worldwide problem. Previous studies show Chinese herbs have been used as a potential non-antibiotic way to enhance anti-inflammatory and anti-microbial functions of piglets. This study aims to evaluate the effect of Forsythia suspense extract (FSE) as an antibiotics substitute on performance, nutrient digestibility, serum antioxidant capacity, fecal Escherichia coli concentration and intestinal morphology of weaned piglets. The results show that dietary FSE supplementation can substitute antibiotics in improving antioxidant capacity, nutrients digestibility and reducing fecal E. coli content, so as to reduce nitrogen output and diarrhea rate, and eventually enhance growth performance in weaned piglets. Abstract: The aim of this study is to determine the efficiency of Forsythia suspense extract (FSE) as an antibiotics substitute on performance, nutrient digestibility, serum antioxidant capacity, fecal Escherichia coli concentration and intestinal morphology of weaned piglets. A total of 108 Duroc × (Landrace × Yorkshire) weaned piglets (28 days (d) weaned, average body weight of 8.68 ± 1.36 kg) were randomly assigned into three dietary treatments, six pens per treatment, three barrows and three gilts per pen. The treatments contained a corn-soybean meal basal diet (CTR), an antibiotic diet (basal diet + 75 mg/kg chlortetracycline; CTC), and an FSE diet (basal diet + 200 mg/kg FSE; FSE). The experiment included phase 1 (d 1 to 14), phase 2 (d 15 to 28) and phase 3 (d 29 to 35). Compared with CTR, piglets fed FSE show improved (p < 0.05) average daily gain (ADG) and average daily feed intake in phase 2, as well as enhanced (p < 0.05) ADG from day 15 to 35 and day 1 to 28. Piglets supplemented with CTC and FSE showed a reduced (p < 0.05) diarrhea rate in phase 1, while piglets fed FSE showed enhanced (p < 0.05) apparent total tract digestibility (ATTD) of dry matter, organic matter, crude protein and gross energy, as well as lower (p < 0.05) nitrogen output in phase 2 compared with CTR and CTC. The content in the form of Colony-Forming Units (CFUs) of fecal E. coli on day 14 and 28 was lower (p < 0.05) in piglets fed FSE in comparison with CTR. The contents of total antioxidant capacity, superoxide dismutase and catalase in serum are enhanced (p < 0.05) compared with CTR and CTC, whereas the concentration of malondialdehyde in serum was decreased (p < 0.05) for piglets fed FSE on day 28 compared with CTC. The villus height to crypt depth ratio in ileum was numerically higher (p < 0.05) in piglets fed FSE in comparison with CTR. In conclusion, dietary FSE supplementation could substitute CTC in improving antioxidant Animals 2019, 9, 729 2 of 12 capacity, nutrients digestibility and reducing fecal E. coli content, so as to reduce nitrogen output and diarrhea rate, and eventually improve performance in weaned piglets.
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Animals 2019, 9, 729; doi:10.3390/ani9100729 www.mdpi.com/journal/animals
Article
Effects of Forsythia Suspense Extract as an Antibiotics
Substitute on Growth Performance, Nutrient
Digestibility, Serum Antioxidant Capacity,
Fecal Escherichia coli Concentration and Intestinal
Morphology of Weaned Piglets
Shenfei Long
, Li Liu
, Sujie Liu, Shad Mahfuz and Xiangshu Piao *
State Key laboratory of Animal Nutrition, College of Animal Science and Technology,
China Agricultural University, Beijing 100193, China; longshenfei@cau.edu.cn (S.F.L.);
jiahao6468@163.com (L.L.); heiluobo12300@163.com (S.J.L.); shadmahfuz@yahoo.com (S.M.)
* Correspondence: piaoxsh@cau.edu.cn; Tel.: +86-10-62733588; Fax: +86-10-62733688
These two authors contributed equally to this work.
Received: 30 August 2019; Accepted: 23 September 2019; Published: 26 September 2019
Simple Summary: Weaning stress may reduce feed intake, weight gain and health status of piglets.
Antibiotics are used to overcome post-weaning disorders. However, the abuse of antibiotics in pig
feed has become a worldwide problem. Previous studies show Chinese herbs have been used as a
potential non-antibiotic way to enhance anti-inflammatory and anti-microbial functions of piglets.
This study aims to evaluate the effect of Forsythia suspense extract (FSE) as an antibiotics substitute
on performance, nutrient digestibility, serum antioxidant capacity, fecal Escherichia coli
concentration and intestinal morphology of weaned piglets. The results show that dietary FSE
supplementation can substitute antibiotics in improving antioxidant capacity, nutrients digestibility
and reducing fecal E. coli content, so as to reduce nitrogen output and diarrhea rate, and eventually
enhance growth performance in weaned piglets.
Abstract: The aim of this study is to determine the efficiency of Forsythia suspense extract (FSE) as an
antibiotics substitute on performance, nutrient digestibility, serum antioxidant capacity, fecal
Escherichia coli concentration and intestinal morphology of weaned piglets. A total of 108 Duroc ×
(Landrace × Yorkshire) weaned piglets (28 days (d) weaned, average body weight of 8.68 ± 1.36 kg)
were randomly assigned into three dietary treatments, six pens per treatment, three barrows and
three gilts per pen. The treatments contained a corn-soybean meal basal diet (CTR), an antibiotic
diet (basal diet + 75 mg/kg chlortetracycline; CTC), and an FSE diet (basal diet + 200 mg/kg FSE;
FSE). The experiment included phase 1 (d 1 to 14), phase 2 (d 15 to 28) and phase 3 (d 29 to 35).
Compared with CTR, piglets fed FSE show improved (p < 0.05) average daily gain (ADG) and
average daily feed intake in phase 2, as well as enhanced (p < 0.05) ADG from day 15 to 35 and day
1 to 28. Piglets supplemented with CTC and FSE showed a reduced (p < 0.05) diarrhea rate in phase
1, while piglets fed FSE showed enhanced (p < 0.05) apparent total tract digestibility (ATTD) of dry
matter, organic matter, crude protein and gross energy, as well as lower (p < 0.05) nitrogen output
in phase 2 compared with CTR and CTC. The content in the form of Colony-Forming Units (CFUs)
of fecal E. coli on day 14 and 28 was lower (p < 0.05) in piglets fed FSE in comparison with CTR. The
contents of total antioxidant capacity, superoxide dismutase and catalase in serum are enhanced
(p < 0.05) compared with CTR and CTC, whereas the concentration of malondialdehyde in serum was
decreased (p < 0.05) for piglets fed FSE on day 28 compared with CTC. The villus height to crypt
depth ratio in ileum was numerically higher (p < 0.05) in piglets fed FSE in comparison with CTR.
In conclusion, dietary FSE supplementation could substitute CTC in improving antioxidant
Animals 2019, 9, 729 2 of 12
capacity, nutrients digestibility and reducing fecal E. coli content, so as to reduce nitrogen output
and diarrhea rate, and eventually improve performance in weaned piglets.
Keywords: Forsythia suspense extract; performance; serum antioxidant status; Escherichia coli
1. Introduction
Weaning is a stressful challenge for piglets because of the sudden changes of physiology and
surrounding environment. These weaning stresses, usually presented as oxidative stress [1], may
reduce antioxidant status, immunity and intestinal functions, which results in a reduction in feed
intake, weight gain and health of piglets, as well as an increase in diarrhea incidence, morbidity and
mortality [2]. To overcome these post-weaning disorders caused by oxidative stress, researchers
report that the use of antibiotics, such as chlortetracycline (CTC), as in-feed supplements after
weaning may help enhance weight gain by 16% and feed utilization by 7%, as well as reduce
morbidity and mortality approximately 50% for weaned piglets [3,4]. However, the abuse or misuse
of antibiotics in piglets’ feed can result in bacteria resistant to antibiotics and lead to potential residues
in animal products (such as pork) and in the environment, which may enhance the possibility of
antibiotic-resistant infections in humans [5]. Therefore, the European Union, the United States and
many other countries have reduced or prohibited the use of antibiotics in animal feed and found
appropriate alternatives for antibiotics.
Studies in our labs have demonstrated that essential oils [6], essential oils combined with mixed
organic acids [7], probiotics [8], chito-oligosaccharide [9] as well as natural plant herbs [10] can
potentially serve as antibiotic substitutes. Currently, the practice of using traditional herbal medicine
is gaining more attention worldwide in animal health care systems [11]. The addition of traditional
Chinese herbs, especially Coptis chinensis and Forsythia suspense, have been used a potential non-
antibiotic way to enhance anti-inflammatory and anti-microbial function, antioxidant status and
performance in livestock [10,12,13].
The fruit or leaf extract of Forsythia suspensa Vahl (Oleaceae) could be widely used as Chinese
medicine to help treat some infections, including pharyngitis, nephritis, febrile erysipelas, ulcers,
tonsillitis, gonorrhea and acute respiratory syndrome [14]. Previous studies in our lab have
demonstrated that lignan, phenethyl alcohol glycoside, volatile oil as well as pentacyclic triterpenoids
are the major active compounds of Forsythia suspensa extract (FSE) [15,16], which has proven to have
anti-oxidant [17], anti-bacterial [12,18], anti-inflammatory [19] and anti-allergy [20] effects. Currently,
our lab has used different stress models and different animal categories (e.g., piglets, broilers, laying
hens and mice) to demonstrate the antioxidant properties and immune enhancement functions of
FSE. Studies also show FSE can enhance performance by modulating intestinal permeability,
antioxidant status and immune function in animals combined with chito-oligosaccharide [13,19] or
berberine [12]. However, there are few data to clarify the possibility of FSE as an antibiotic substitute
and the possible mechanism functions of FSE. Therefore, the objective of this study is to evaluate the
efficiency of FSE as an antibiotics substitute on performance, serum antioxidant status, fecal
Escherichia coli content and intestinal morphology in weaned piglets.
2. Materials and Methods
The study was carried out at the Animal Experimental Base (Fengning, Hebei, China) in the
National Feed Engineering Technology Research Center of the Ministry of Agriculture Feed Industry
Center. All the experimental procedures and operations used in the management and care of piglets
were in agreement with the China Agricultural University Laboratory Animals Welfare and Animal
Experimental Ethical Inspection (Beijing, China; No. AW09089102-1).
Animals 2019, 9, 729 3 of 12
2.1. Experimental Products
Dried and ground forsythia fruits (about 100 g) were prepared and extracted by 80% ethanol
(500 mL), sonicated for 1 h and then filtered. Ethanol was used to extract the residue twice and then
rotary vaporization (Buchi, Rotavapor R-124, Flawil, Switzerland) was utilized to dry and combine
the filtrates. The main functional ingredients in FSE are forsythoside A (1.65%), phillyrin (8.17%),
forythialan A (4.13%) and phillygenin (1.67%) [10]. An additional antibiotic mixture
(chlortetracycline, CTC) was produced by Beijing Tongli Xing Department of Agricultural Science
and Technology Company Limited (Beijing, China).
2.2. Experimental Animals, Management and Design
A total of 108 Duroc × (Landrace × Yorkshire) weaned piglets (28 days (d) weaned, average body
weight of 8.68 ± 1.36 kg) were randomly assigned into 3 dietary treatments, 6 pens per treatment, 3
barrows and 3 gilts per pen. The treatments contained a corn-soybean meal basal diet (CTR), an
antibiotic diet (basal diet + 75 mg/kg chlortetracycline; CTC), and an FSE diet (basal diet + 200 mg/kg
FSE; FSE). The experiment included phase 1 (d 1 to 14), phase 2 (d 15 to 28) and phase 3 (d 29 to 35).
As shown in Table 1, nutrients in the diet met the recommended requirements (National Research
Council, NRC, 2012) [21].
Table 1. Composition and nutrient levels of basal diets (%, as-fed basis).
Ingredients Day 1 to 14 Day 15 to 35
Corn 55.64 56.00
Soybean meal, 43% 18.00 20.00
Extruded soybean 12.00 10.00
Spray dried plasma protein 4.00 0.00
Fish meal 2.00 4.00
Whey powder 2.00 5.50
Soy oil 2.80 1.73
Dicalcium phosphate 0.90 0.52
Limestone 1.12 0.80
Salt 0.30 0.30
L-lysine HCl, 78% 0.22 0.26
DL-Methionine, 98% 0.10 0.06
L-Threonine, 98% 0.01 0.07
L-Tryptophan, 98% 0.00 0.01
Zinc oxide 0.16 0.00
Chromic oxide 0.25 0.25
Vitamin-mineral premix 1 0.50 0.50
Calculated nutrient levels
Digestible energy, kcal/kg 3541 3490
Crude protein 21.47 20.05
Calcium 0.80 0.70
Digestible phosphorus 0.40 0.33
Standardized ileal digestible lysine 1.35 1.23
Standardized ileal digestible methionine 0.39 0.36
Standardized ileal digestible threonine 0.79 0.73
Standardized ileal digestible tryptophan 0.23 0.20
Analyzed nutrient levels
Gross energy, kcal/kg 4016 3996
Crude protein 21.56 19.78
Calcium 0.82 0.72
Gross phosphorus 0.60 0.55
Animals 2019, 9, 729 4 of 12
Lysine 1.52 1.42
Methionine 0.45 0.42
Threonine 0.90 0.87
Tryptophan 0.27 0.25
1 premix for each kg diet: vitamin A, 12,000 IU; vitamin D3, 2500 IU; vitamin E, 30 IU; vitamin K3, 30
mg; vitamin B12, 12 μg; riboflavin, 4 mg; pantothenic acid, 15 mg; nicotinic acid, 40 mg; choline
chloride, 400 mg; folic acid, 0.7 mg; vitamin B1, 1.5 mg; vitamin B6, 3 mg; biotin, 0.1 mg; manganese,
40 mg; iron, 90 mg; zinc, 100 mg Mg; copper, 8.8 mg; iodine, 0.35 mg; selenium, 0.3 mg.
All the piglets were raised in experimental pens (1.2 m × 2 m) fitted with a duckbill drinker, an
adjustable stainless steel feeder and plastic slatted floors. The piglets were given access to water and
fed ad libitum in powder form. Inside the pen, these piglets also had free access to feed (in mash
form) and water ad libitum. The environment in the pig house, including the contents of carbon
dioxide and ammonium in the air, ventilation intensity, humidity and temperature, was controlled
automatically. The average temperature in house was controlled at 24–26 °C, while the relative
humidity was maintained at 60%–70%. In order to prevent disease, the experimental house was
cleaned every day and the immunization procedure was conducted every week. After 12 h of
starvation, the individual weight of piglets and the feed weight of each pen were weighed on day 0,
14, 28 and 35 to calculate the average daily gain (ADG), average daily feed intake (ADFI) and feed
efficiency (FE, ADFI/ADG). From day 0 to 28, the diarrhea score was monitored according to the
previously described system [22] from 1 to 5: 1, hard firm feces (rarely seen); 2, slightly soft feces; 3,
soft, partially formed feces; 4, loose, semi-liquid feces (diarrhea); 5, watery, mucus-like feces (severe
diarrhea). The determination of diarrhea rate was mainly dependent on the average diarrhea score
following the formula: diarrhea rate (%) = diarrhea days × the number of diarrhea pigs/(experiment
days × the total number of pigs) [23].
2.3. Experimental Sample Collection and Analysis
During this experiment, a total of 2 kg representative feed samples were collected weekly. From
day 12 to 14 and day 26 to 28, the rectal palpation was used to make sure approximately 100 g of fresh
feces were collected using the grab sample technique. All the fecal samples were frozen at 20 °C
immediately after collection until analysis. The feces collected after 3 days were pooled by pen and
dried at 65 °C for 72 h. Before analysis, all these dried feces and feed samples were ground to pass
through a 1-mm sieve.
The dry matter (DM), ether extract (EE) and crude protein (CP) of the feed and fecal samples
were measured using the methods of Association of Official Agricultural Chemists (AOAC) [24]. The
gross energy (GE) in feed and fecal samples was determined by an automatic isoperibolic oxygen
bomb calorimeter (Parr 1281, Automatic Energy Analyzer; Moline, IL, USA). Moreover, an atomic
absorption spectrophotometer (Z-5000; Hitachi, Tokyo, Japan) was used to determine the content of
chromium in feed and fecal samples. Organic matter (OM) was calculated as 1 ash content (DM
base). The calculation formula for total carbohydrates was as follows: the calculation = dry matter
crude protein ether extract ash [25]. Nutrient digestibility was determined by the equation as
follows: apparent total tract digestibilitynutrient (ATTD) = 1 (Crdiet × nutrientfeces)/(Crfeces × nutrientdiet).
The manure nitrogen output from piglets fed FSE during a 28-d period of the experiment was
calculated by the equation as follows: fecal nitrogen (N) excretion per weight gain (g/kg) = (N intake
(g/d) × (100 ATTD of N)) / ([100 × ADG (kg/d)).
For the determination of fecal microbiota, the fresh fecal samples (about 100 g) of piglets in the
CTR and FSE groups collected on day 14 and day 28 were first thawed at room temperature. A total
of 1 g of fresh fecal sample was taken and transferred into a 9-mL diluent tube and then diluted 6
times serially in order to make sure every sample was fully dissolved. The test of fecal E. coli
concentrations in fresh fecal samples was carried out within a day after collection. The total content
of E. coli was determined using Maconkey agar to plate 0.1 mL diluent. An electro-heating standing-
Animals 2019, 9, 729 5 of 12
temperature cultivator (37 °C) was used to incubate all the petri dishes for 24 h. Before statistical
analysis, the fecal E. coli concentrations were transformed (Log).
After starvation for 12 h, approximately 8 mL of blood was collected from a piglet near the
average group body weight in each pen via jugular vein puncture into a vacutainer at 7:00 a.m. on
day 28 (Becton Dickinson Vacutainer Systems, Franklin Lakes, NJ, USA). After stewing for 3 h, all the
collected blood samples were centrifuged at 3000× g for 15 min at 4 °C to get the serum samples,
which were also stored at 20 °C until analysis. Estimation of triglyceride (TG) and blood urea
nitrogen (BUN) contents in serum were conducted by Hitachi 7600 Automatic Biochemical
Instrument. An ELISA kit (IgG, IgM and IgA quantitation kit; Bethyl Laboratories, Inc., Montgomery,
TX, USA) was used to determine the concentrations of serum immunoglobulins (including
immunoglobulin G, immunoglobulin M and immunoglobulin A). Determination of total antioxidant
capacity (T-AOC), catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GSH-Px)
and malondialdehyde (MDA) levels in serum were conducted by spectrophotometric methods using
a spectrophotometer (Leng Guang SFZ1606017568, Shanghai, China) following the instructions of the
kit’s manufacturer (Nanjing Jiancheng Bioengineering Institute, Nanjing, China).
On day 28, the aseptic duodenal, jejunal and ileal samples (about 5 cm fragment in the middle
of each intestine, duodenum was selected as the proximal 1/3 of the small intestine, jejunum as the
1/3 mid and ileum as 1/3 distal part) were collected from slaughtered barrows (near the average group
body weight) selected in each pen for the determination of intestinal morphology. Then, 10% neutral
buffered formalin was used to fix rapidly these histological samples for slicing. After 48 h of fixation,
the sections of intestinal tissues were washed, excised, dehydrated, as well as embedded in the
paraffin wax, and then 5 transverse sections were sliced, installed on glass slides and dyed with eosin
and hematoxylin. At least 20 orientated villi and their adjoining crypts were selected randomly on
each slice and measured to calculate the average villus height and crypt depth via a light microscope
in small caps using a calibrated 10-fold eyepiece graticule. The ratio of villus height to crypt depth
was calculated and used for further analysis.
2.4. Statistical Analysis
The mixed model of SAS (version 9.2, 2008) [26] was used for variance analysis of all the data.
The dietary treatments were fixed e ffects, while sex and body weight o f pigs were the random effects.
For the analysis of growth performance and diarrhea rate, the pen was treated as the statistical unit,
whereas for the analysis of other data, individual piglets were taken as a statistical unit. The Student–
Newman–Keul multiple range test was used for determining the statistical differences among all the
treatments. Significant difference between the mean value was defined at p 0.05, while a trend for
the significance between the mean value was designated at 0.05 < p 0.10.
3. Results
3.1. Performance and Diarrhea Rate of Piglets
The growth performance (ADG, ADFI and FE) and diarrhea rate are shown in Table 2.
Compared with CTR, the ADG and ADFI are improved (p < 0.05) approximately 19% and 17% in
piglets supplemented with an FSE diet from day 15 to 28, and the ADG is enhanced (p < 0.05) about
12% and 13% by FSE for piglets from day 1 to 28 and day 15 to 35. Meanwhile, piglets fed an FSE diet
also showed a tendency in increasing ADG from day 1 to 35 in comparison with CTR (p = 0.10). The
FE was not affected by any dietary additives. Compared with CTR, piglets fed CTC and FSE had a
reduced (p < 0.05) diarrhea rate of about 77% and 61% from day 1 to 14.
Animals 2019, 9, 729 6 of 12
Table 2. Effects of Forsythia suspense extract on performance and diarrhea rate in weaned piglets.
Item CTR 1 CTC 1 FSE 1 SEM p-Value
day 1 body weight 8.68 8.68 8.68 0.01 0.85
day 1 to 14
Average daily gain, g 404 418 422 14.84 0.68
Average daily feed intake, g 748 783 773 39.57 0.82
Feed efficiency, g gain/g feed 0.55 0.54 0.55 0.03 0.97
Diarrhea rate, % 3.09 a 0.71
b 1.19
b 0.44 0.01
day 15 to 28
Average daily gain, g 453 b 472
b 540
a 14.11 <0.01
Average daily feed intake, g 903 b 956
a,b 1060
a 37.00 0.04
Feed efficiency, g gain/g feed 0.50 0.49 0.51 0.02 0.79
Diarrhea rate, % 4.05 4.28 3.57 1.32 0.93
day 1 to 28
Average daily gain, g 428 b 445
b 481
a 7.80 <0.01
Average daily feed intake, g 825 870 916 30.13 0.16
Feed efficiency, g gain/g feed 0.52 0.51 0.53 0.02 0.82
Diarrhea rate, % 3.57 2.50 2.38 0.74 0.49
day 15 to 35
Average daily gain, g 561 b 587
b 633
a 16.41 0.04
Average daily feed intake, g 1005 1031 1075 24.89 0.20
Feed efficiency, g gain/g feed 0.56 0.57 0.59 0.02 0.56
day 29 to 35
Average daily gain, g 670 702 726 30.29 0.45
Average daily feed intake, g 1107 1106 1090 37.96 0.94
Feed efficiency, g gain/g feed 0.60 0.63 0.67 0.02 0.23
day 1 to 35
Average daily gain, g 549 574 603 17.40 0.10
Average daily feed intake, g 966 988 1003 24.42 0.58
Feed efficiency
,
g gain/g feed 0.57 0.58 0.60 0.02 0.37
SEM means standard error of mean. a,b Different superscripts within a row indicate a significant
difference (p < 0.05). 1 CTR: control; CTC: chlortetracycline; FSE: Forsythia suspense extract.
3.2. The ATTD of Nutrients and Nitrogen Output
The ATTD of nutrients is presented in Table 3. In phase 1, piglets fed FSE showed increased (p < 0.05)
ATTD of DM, OM, CP and GE by approximately 7%, 6%, 9% and 7%, respectively compared with
CTR and CTC. In phase 2, there was a tendency of improvement on the ATTD of CP (p = 0.06) and
GE (p = 0.10) in piglets supplemented with FSE in comparison with CTR and CTC.
The manure nitrogen output from piglets fed FSE during a 28-d period experiment is presented
in Figure 1; piglets fed FSE have lower (p < 0.05) nitrogen output compared with CTR and CTC.
Animals 2019, 9, 729 7 of 12
Table 3. Effects of Forsythia suspense extract on apparent total tract digestibility of nutrients in weaned
piglets (%).
Items CTR 1 CTC 1 FSE 1 SEM p-Value
day 14
Dry matter 81.63 b 82.92
b 87.31
a 0.91 <0.01
Organic matter 83.93 b 85.08
b 88.72
a 0.81 <0.01
Crude protein 75.47 b 76.94
b 82.51
a 1.34 0.01
Gross energy 81.16 b 82.65
b 87.07
a 0.92 <0.01
Total carbohydrates 89.05 b 89.96
b 92.37
a 0.56 <0.01
day 28
Dry matter 77.21 74.83 78.10 1.03 0.12
Organic matter 80.02 78.10 81.01 0.92 0.13
Crude protein 66.43 62.83 68.81 1.48 0.06
Gross energy 77.06 74.77 78.95 1.18 0.10
Total carbohydrates 86.08 85.05 86.85 0.71 0.25
SEM means standard error of mean. a,b Different superscripts within a row indicate a significant
difference (p < 0.05). 1 CTR: control; CTC: chlortetracycline; FSE: Forsythia suspense extract.
Figure 1. Manure nitrogen (N) output from piglets fed diets based on corn soybean meal diet
supplemented with 75 mg/kg chlortetracycline or 200 mg/kg Forsythia suspense extract during a 28-d
period experiment. Values are least square means ± SEM, n = 6/treatment. a,b Means without common
letters differ significantly (p < 0.05).
3.3. Fecal Escherichia coli Contents
The fecal E. coli content on day 14 and 28 is given in Table 4. The content [in the form of the
Colony-Forming Units (CFUs)] of E. coli in feces is lower (p < 0.05) by approximately 59% and 36% on
day 14 and 28, respectively in piglets fed FSE in comparison with CTR.
Animals 2019, 9, 729 8 of 12
Table 4. Effects of Forsythia suspense extract on Escherichia coli content in feces of weaned piglets (108
CFUs)/g).
Items CTR 1 FSE 1 SEM p-Value
day 14
Escherichia coli 28.75 a 14.08
b 1.55 0.02
day 28
Escherichia coli 21.52 a 13.88
b 0.83 0.02
SEM means standard error of mean. CFUs means Colony-Forming Units. a,b Different superscripts
within a row indicate a significant difference (p < 0.05). 1 CTR: control; FSE: Forsythia suspense extract.
3.4. Serum Metabolic Profile, Immunity and Antioxidant Indices
Effects of FSE on serum metabolic profile, immunity and antioxidant status of weaned piglets
on day 28 is shown in Tables 5–7. Compared with CTR, there is no significant difference of serum
metabolic profile and immunoglobulin levels in piglets fed diets supplemented with FSE. However,
the serum contents of T-AOC, SOD and CAT are enhanced (p < 0.05) in piglets fed FSE compared
with those fed CTR and CTC, whereas the concentration of MDA is decreased (p < 0.05) in piglets fed
FSE on day 28 in comparison with CTC.
Table 5. Effects of Forsythia suspense extract on serum metabolic profile of weaned piglets on day 28
(mmol/L).
Items CTR 1 CTC 1 FSE 1 SEM p-Value
Triglyceride 1.79 1.99 1.99 0.08 0.20
Blood urea nitrogen 2.36 3.11 2.51 0.61 0.67
SEM means standard error of mean. 1 CTR: control; CTC: chlortetracycline; FSE: Forsythia suspense
extract.
Table 6. Effects of Forsythia suspense extract on serum immunoglobulin levels of weaned piglets on
day 28 (g/L).
Items CTR 1 CTC 1 FSE 1 SEM p-Value
Immunoglobulin A 0.97 0.94 1.09 0.09 0.50
Immunoglobulin G 21.16 20.85 21.23 0.51 0.85
Immunoglobulin M 2.33 2.37 2.40 0.04 0.47
SEM means standard error of mean. 1 CTR: control; CTC: chlortetracycline; FSE: Forsythia suspense
extract.
Table 7. Effects of Forsythia suspense extract on antioxidant status in serum of weaned piglets on day 28.
Items CTR 1 CTC 1 FSE 1 SEM p-Value
T-AOC 2, U/mL 13.53 b 10.20
c 14.43
a 0.25 <0.01
SOD 2, U/mL 73.04 b 64.79
c 82.36
a 1.88 <0.01
CAT 2
,
U/mL 44.49 b 36.61
c 63.24
a 2.06 <0.01
GSH-Px 2
,
U/mL 809 796 843 14.86 0.15
MDA 2, nmol/mL 4.91 b 5.60
a 4.41
b 0.56 <0.01
SEM means standard error of mean. a,b Different superscripts within a row indicate a significant
difference (p < 0.05). 1 CTR: control; CTC: chlortetracycline; FSE: Forsythia suspense extract. 2 T-AOC:
total antioxidant capacity; SOD: superoxide dismutase; CAT: catalase; GSH-Px: glutathione
peroxidase; MDA: malondialdehyde.
3.5. Intestinal Morphology
The effects of FSE on intestinal morphology of weaned piglets on day 28 are shown in Table 8.
There is a decreased tendency of crypt depth in ileum of piglets fed FSE (p = 0.09), while the villus
Animals 2019, 9, 729 9 of 12
height to crypt depth ratio is numerically higher (p < 0.05) in piglets fed FSE in comparison with CTR.
The villus height of piglets fed FSE are numerically higher (p > 0.05) at approximately 11% in
duodenum and 26% in jejunum, respectively.
Table 8. Effects of Forsythia suspense extract on intestinal morphology of weaned piglets on day 28.
Items CTR
1 CTC 1 FSE 1 SEM p-Value
Duodenum
Villus height 468 561 519 53.40 0.53
Crypt depth 314 264 274 64.70 0.85
Villus height
/
crypt depth 1.55 2.55 2.08 0.52 0.47
Jejunum
Villus height 419 496 526 46.41 0.34
Crypt depth 269 280 237 39.94 0.74
Villus height/crypt depth 1.60 1.81 2.36 0.23 0.17
Ileum
Villus height 488 453 440 43.18 0.74
Crypt depth 304 216 180 29.73 0.09
Villus height
/
crypt depth 1.64 b 2.14 a,b 2.52 a 0.10 <0.01
SEM means standard error of the mean. a,b Different superscripts within a row indicate a significant
difference (p < 0.05). 1 CTR: control; CTC: chlortetracycline; FSE: Forsythia suspense extract.
4. Discussion
Weaning stress may cause a reduction of growth rate and feed intake in piglets, while current
results show dietary FSE supplementation can enhance ADG and ADFI in phase 2, but there is no
difference of performance among dietary treatments in phase 1. Similar results are also shown in the
study by Han et al. [18], which demonstrated that during the first period, performance has no
difference in the FSE group, while it experiences a significant enhancement during the finisher and
overall phase in broilers. This indicates that the beneficial effect of FSE on piglets may relate to its
cumulative effect in animals. However, according to the study of Zhao et al. [19], dietary
supplementation with 100 mg/kg FSE can improve ADG and FE in the first 2 weeks. These different
findings may relate to the amount and composition of FSE in different studies. The present study
showed that there is no significant difference of FE between treatments, while other studies show
dietary plant polyphenols supplementation can improve the FE in pigs via the improvement of
nutrients digestibility [27] and the enhancement of health status via inhibiting inflammation [28].
These contradictory functions of FSE on FE in different studies may also relate to the type, additive
amount and chemical composition of Chinese plant polyphenols. The current study also shows that
the effects of FSE on enhancing growth performance is better than CTC, which is partly in line with
the study of Han et al. [18], who also indicated that FSE has the potential to replace antibiotics in
improving the performance and intestinal health of animals. The reason for the improved
performance may also be due to the decreased diarrhea rate and improved nutrient utilization of
piglets fed an FSE diet.
After weaning, piglets are susceptible to disease due to environmental changes, which usually
cause severe post-weaning diarrhea. The present study shows that piglets fed a CTC and FSE diet
experienced a significant reduction in diarrhea rates in phase 1 and 2; this could possibly be due to
the lower content of E. coli in feces of piglets fed a CTC and FSE diet since diarrhea caused by E. coli
is a major challenge for post-weaning pigs [8]. The present result is in agreement with the study of
Han et al. [18], who reported that FSE can regulate intestinal flora via reducing the cecal E. coli counts
in vivo and inhibiting the reproduction of E. coli K88, Staphylococcus aureus and salmonella in vitro.
The result may be because polyphenol in FSE can increase the fecal pH value and lower the
concentrations of volatile fatty acids [27]. Another reason may be that the forsythiaside and phillyrin
in FSE have strong broad-spectrum antimicrobial activity [29], which can effectively inhibit E. coli,
Pseudomonas aeruginosa and S. aureus [30,31]. Moreover, the essential oils from FSE have also
Animals 2019, 9, 729 10 of 12
demonstrated their effectiveness in inhibiting the growth of S. aureus, Bacillus subtilis, E. coli, P.
aeruginosa, Candida albicans and Aspergillus Niger [32]. In addition, according to a study by Zhang et
al. [12], FSE may also increase the level of Lactobacillus while reducing the level of E. coli in the cecum
of broilers on day 21 and 42, thus improving the structure of intestinal flora in broilers. In our present
study, we consider the number of CFUs of E. coli only; the differences may not represent a real
reduction in E. coli, therefore, this finding still needs to be further estimated in our following studies.
During the first two weeks after weaning, piglets may face severe challenges when they utilize
nutrients, which is mainly due to disorders in the digestive and absorption systems. In the present
study, the ATTD of nutrients were enhanced in piglets fed an FSE diet in phase 1, which is partly in
agreement with the previous study of Han et al. [18] and Zhang et al. [12]. The digestibility of
nutrients strongly increased in piglets fed FSE compared to CTR in phase 1 and tended to be
enhanced in phase 2, which can normally lead to an improvement of ADG and FE [19]. However, our
study only found the enhancement of ADG in phase 2, from day 15 to 35 and day 1 to 28, which may
be due to that the enhancement of ADFI in phase 2 as well as the difference of the additive amount
and composition of FSE. After weaning within 2 weeks, the digestive system of piglets is not well
developed and Chinese medicine usually has an accumulative effect for animals, which may lead to
the positive effect of FSE on ADG to be easier to find in phase 2, from day 15 to 35 and day 1 to 28 [18].
Yet this finding still remains to be investigated in further study. Moreover, the improved nutrient
digestibility in the current study is in line with the increased villus height to crypt depth ratio and
decreased crypt depth in ileum of piglets fed an FSE diet. This may be because FSE can help improve
small intestinal villus morphology, enhancing the growth of villus as well as the villus hei ght to crypt
depth ratio, which in turn may increase the absorption of DM and CP [12]. In addition, FSE can also
improve the proliferation of peripheral blood lymphocytes and intestinal permeability, so as to
increase the intestinal capacity to utilize nutrients [20]. The higher numerical changes of the villus
height, crypt depth and their ratio in the small intestine probably indicates FSE may benefit and help
in the development of the small intestine in weaned piglets [18]. A possible reason for the obviously
improved nutrient digestibility in the early phase for piglets may be that after weaning, the
development of the intestine and activity of digestible enzymes are poor, while the intestine is better
developed after two weeks in the later phase. The reduction of manure N output from piglets fed
diets based on a corn-soybean meal diet supplemented with FSE is mainly due to the improved ATTD
of CP.
When oxidants and antioxidants are in an unbalanced state (oxidative stress reaction), a large
number of reactive oxygen species (ROS) will be produced. These excessive ROS and free radicals
can lead to lipid peroxidation, DNA damage, cell apoptosis or cell cycle arrest, eventually leading to
cell death [33]. In the present study, the contents of T-AOC, SOD and CAT are enhanced, whereas the
concentration of MDA is decreased in piglets fed an FSE diet. This may because FSE could be an effective
antioxidant in vitro and in vivo. In vitro studies have shown that the scavenging rates of 100 g/mL and
250 g/mL FSE for 1,1-diphenyl-2-trinitrophenylhydrazine (DPPH) free radical can reach 77.2% and
81.3% respectively, which are comparable to vitamin C [17]. Moreover, the phenolic hydroxyl ortho-
position on the phenyl ring of forsythiaside in FSE has a strong antioxidant and free radical
scavenging ability, which can effectively protect cells from hydrogen peroxide-induced cell damage
(reducing ROS and MDA levels) and mitochondrial-dependent cell apoptosis [10]. In vivo studies
have shown that FSE can effectively alleviate the oxidative damage of diquat to Sprague-Dawley (SD)
rats, reduce MDA content and inflammatory factors in the liver and serum [10], which is mainly
because forsythiaside in FSE can activate non-enzymatic system, improve total antioxidant capacity
and increase the expression of antioxidant enzymes in cells by promoting the level of nuclear factor
erythroid-2-related factor 2 in the nucleus [29], so as to activate antioxidant enzymes system (such as
SOD, CAT and GSH-Px). Moreover, the polyphenols in FSE can also play an important role in
enhancing the activities of antioxidant enzymes in the blood, liver, spleen and kidneys, which largely
contributes to improving the health status and growth performance of weaned piglets [34].
Animals 2019, 9, 729 11 of 12
5. Conclusions
In conclusion, dietary Forsythia suspense extract (200 mg/kg) supplementation as a substitute for
chlortetracycline can help improve performance, nutrient digestibility, serum antioxidant capacity
and intestinal morphology as well as reduce the content of Escherichia coli in the feces of weaned pigs.
Author Contributions: For this paper, conceptualization, S.L. (Shenfei Long) and X.P.; data curation, S.L.
(Shenfei Long); formal analysis, S.L. (Shenfei Long); funding acquisition, X.P.; investigation. L.L.; methodology,
L.L.; project administration, S.L. (Sujie Liu); resources, S.L. (Sujie Liu); software, S.M.; supervision, X.P.;
validation, X.P.; visualization, X.P.; writing—original draft preparation, S.L. (Shenfei Long) and L.L.; writing—
review and editing, S.L. (Shenfei Long) and S.M.
Funding: This research was funded by the National Natural Science Foundation of China (31772612) and CARS 35.
Acknowledgments: We want to thank the support of the National Natural Science Foundation of China
(31772612) and CARS 35.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to
publish the results.
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... Studies showed that some functional nutrients or seaweed extracts could enhance the body's immune and antioxidant functions of piglets through maternal transmission (18)(19)(20)(21). In our previous studies, we also found that dietary supplementation with FSE could effectively modulate intestinal morphology and microbial community in broilers or weaned pigs (22,23). While diet supplemented with FSE in late gestating sows could help to increase the nutrient utilization, antioxidant status, and inflammatory responses, and eventually alleviate oxidative stress during farrowing and improve the reproductive performance of sows (24). ...
... This finding might be due to the effect of polyphenol in forythialan A, forsythiaside A, phillygenin, and phillyrin on improving immunity and antioxidant capacity in pigs. Moreover, similar to the current finding, previous studies in our lab also demonstrated that FSE could lead to better ADG of weaned piglets or broilers, especially in the later phases, which was mainly due to its accumulation effect and beneficial effects on improving nutrient digestibility, immunoglobulin, and intestinal health (14,23). The appearance of oxidative stress in the perinatal period of animals made the energy used for synthesizing milk or other production turn to the synthesis of antioxidant substances, which reduced the production efficiency and the quality of milk due to the accumulation of oxidative substances (40). ...
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... Forsythia suspensa is the one of Chinese natural herbs, which has strong antioxidant, antibacterial, antiviral, and anti-inflammatory properties (5). Previous studies in our lab have demonstrated that F. suspensa extract (FSE) improved the performance and nutrient digestibility of weaned piglets by improving antioxidant capacity, immune function, and intestinal morphology (6,7). FSE could improve performance and antioxidant enzyme activities in broilers under heat or high-density-induced oxidative stress (8,9). ...
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... Phytochemicals, such as polyphenols, terpenes, and flavonoids are considered bioactive compounds with multiple biological effects including antioxidant, anti-inflammatory, antimicrobial, and anti-tumor (3)(4)(5). With the prohibition of using antibiotics in feed (6), plant extracts have been expected to replace antibiotics and thus become a hot spot in animal nutrition research (7). Earlier, various herbs have been proven to attenuate oxidative stress and improve meat quality in poultry (2,8,9). ...
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These studies evaluated the effects of probiotics (PB) as a potential substitute for antibiotics (AB) on diarrhea in relation to immune responses and intestinal health in weaned pigs challenged with enterotoxigenic Escherichia coli (ETEC) K88 (Exp. 1) and the effects of PB on performance and nutrient digestibility in weaned pigs (Exp. 2). In Exp. 1, 24 weaned barrows (4.9 ± 0.4 kg initial BW) were randomly assigned to 1 of 4 treatments. The treatments consisted of pigs fed an unsupplemented corn–soybean meal basal diet and not challenged (NON-C) or challenged with ETEC K88 (CHA-C) on d 9 and pigs fed the same basal diet supplemented with AB (100 mg/kg zinc bacitracin, 50 mg/kg colistin sulfate, and 100 mg/ kg olaquindox; CHA-AB) or 500 mg/kg PB (Bacillus licheniformis and Saccharomyces cerevisiae; CHA-PB) and challenged with ETEC K88 on d 9. In Exp. 2, 108 weaned pigs (7.5 ± 0.9 kg initial BW) not challenged with ETEC K88 were randomly assigned to 1 of 3 treatments, including an AB-free basal diet (CON) and the basal diet with AB (ABD) or 500 mg/ kg PB supplementation (PBD). In Exp. 1, after challenge, CHA-C decreased (P < 0.05) ADG and ADFI, whereas CHA-AB and CHA-PB revealed no significant change compared with NON-C. Compared with CHA-C, CHA-AB and CHA-PB improved (P < 0.05) ADG and ADFI and decreased (P < 0.05) the diarrhea incidence in pigs. Mucosal secretory Ig A contents in the jejunum and ileum were greater in CHA-C than in NON-C (P < 0.05) and lower than in CHA-PB (P < 0.05). The diet containing PB alleviated the increase in the endotoxin and diamine oxidase concentration and cecal E. coli count (P < 0.05) and the decrease in intestinal villus height, cecal Lactobacillus count, and jejunal mucosal occludin protein abundance (P < 0.05). In Exp. 2, dietary supplementation with AB and PB had positive effects on ADG and feed efficiency (P < 0.05). Compared with CON, apparent digestibility of nutrients in PBD was improved (P < 0.05). Collectively, PB supplementation protected the pigs against ETEC K88 infection by enhancing immune responses and attenuating intestinal damage and improved the performance and nutrient digestibility of weaned pigs. Therefore, PB could be a potential effective alternative to AB for ameliorating diarrhea and improving performance in weaned pigs. © 2017 American Society of Animal Science. All rights reserved.
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The objective of this experiment was to evaluate the effect of two mixed organic acids (OA) on performance, serum immunity, intestinal morphology and microbiota of weaned pigs in comparison with antibiotic growth promoters (AGP). A total of 144 weaned piglets [Duroc × (Landrace × Yorkshire), average weight 8.63 ± 1.56 kg] were randomly allocated to 1 of 4 dietary treatments with 6 replicate pens per treatment (3 barrows and 3 gilts per pen). The dietary treatments included a corn-soybean basal diet (CTR), AGP diet (CTR + 10 mg/kg zinc bacitracin, 5 mg/kg colistin sulphate and 5 mg/kg olaquindox), Organic acid 1 diet [OA1; CTR + 3000 mg/kg OA1; a synergistic blend of free and buffered short chain fatty acids (mainly formic acid, acetic acid and propionic acid) combined with medium chain fatty acids (MCFA)]. Organic acid 2 diet (OA2; CTR + 2000 mg/kg OA2; a synergistic blend of a phenolic compound, slow release C12, target release butyrate and sorbic acid, MCFA and OA). Compared with CTR, average daily gain (ADG) and feed efficiency (FE) were improved (P < 0.05) by OA2 in phase 2 (d 14–28) and the overall period (d 0–28), and OA1 improved (P < 0.05) FE during the overall period, while AGP increased (P < 0.05) ADG and FE in phase 2. Both OA1 and OA2 reduced (P < 0.05) the incidence of diarrhea and fecal E. coli counts. The apparent total tract digestibility (ATTD) of total carbohydrates, neutral detergent fiber (NDF), acid detergent fiber (ADF) and phosphorus was improved (P < 0.05) by OA2 in phase 1 (d 0–14). In phase 2, OA1 increased (P < 0.05) ATTD of dry matter, total carbohydrates, NDF and ADF while OA2 improved (P < 0.05) ATTD of total carbohydrates, phosphorus and ether extract. Compared with CTR, the concentration of total volatile fatty acid in feces was improved (P < 0.01) in pigs supplemented with AGP, OA1 and OA2. The concentration of IgG, growth hormone, and total antioxidant capacity in serum tended to be higher, and the amount of hydroxyl radicals in serum was lower (P < 0.05) in pigs supplemented with OA2 compared with CTR. Crypt depth in the jejunum for piglets fed with OA2 was lower (P < 0.05), and the ratio of villus height to crypt depth in the jejunum and ileum was greater (P < 0.05) in pigs fed with AGP, OA1 or OA2 than those of CTR. The results from the present research indicate that OA1 and OA2 can be used to replace AGP based on the positive effects on performance, serum immunity, intestinal morphology and microbiota in the weaned piglets.
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Weaning is a critical event in the pig’s life cycle, frequently associated with severe enteric infections and overuse of antibiotics; this raises serious economic and public health concerns. In this review, we explain why gut microbiota dysbiosis, induced by abrupt changes in the diet and environment of piglets, emerges as a leading cause of post-weaning diarrhea, even if the exact underlying mechanisms remain unclear. Then, we focus on nonantimicrobial alternatives, such as zinc oxide, essential oils, and prebiotics or probiotics, which are currently evaluated to restore intestinal balance and allow a better management of the crucial weaning transition. Finally, we discuss how in vitro models of the piglet gut could be advantageously used as a complement to ex vivo and in vivo studies for the development and testing of new feed additives.
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These studies evaluated the effects of probiotics (PB) as a potential substitute for antibiotics (AB) on diarrhea in relation to immune responses and intestinal health in weaned pigs challenged with enterotoxigenic (ETEC) K88 (Exp. 1) and the effects of PB on performance and nutrient digestibility in weaned pigs (Exp. 2). In Exp. 1, 24 weaned barrows (4.9 ± 0.4 kg initial BW) were randomly assigned to 1 of 4 treatments. The treatments consisted of pigs fed an unsupplemented corn-soybean meal basal diet and not challenged (NON-C) or challenged with ETEC K88 (CHA-C) on d 9 and pigs fed the same basal diet supplemented with AB (100 mg/kg zinc bacitracin, 50 mg/kg colistin sulfate, and 100 mg/kg olaquindox; CHA-AB) or 500 mg/kg PB ( and ; CHA-PB) and challenged with ETEC K88 on d 9. In Exp. 2, 108 weaned pigs (7.5 ± 0.9 kg initial BW) not challenged with ETEC K88 were randomly assigned to 1 of 3 treatments, including an AB-free basal diet (CON) and the basal diet with AB (ABD) or 500 mg/kg PB supplementation (PBD). In Exp. 1, after challenge, CHA-C decreased ( < 0.05) ADG and ADFI, whereas CHA-AB and CHA-PB revealed no significant change compared with NON-C. Compared with CHA-C, CHA-AB and CHA-PB improved ( < 0.05) ADG and ADFI and decreased ( < 0.05) the diarrhea incidence in pigs. Mucosal secretory Ig A contents in the jejunum and ileum were greater in CHA-C than in NON-C ( < 0.05) and lower than in CHA-PB ( < 0.05). The diet containing PB alleviated the increase in the endotoxin and diamine oxidase concentration and cecal count ( < 0.05) and the decrease in intestinal villus height, cecal count, and jejunal mucosal occludin protein abundance ( < 0.05). In Exp. 2, dietary supplementation with AB and PB had positive effects on ADG and feed efficiency ( < 0.05). Compared with CON, apparent digestibility of nutrients in PBD was improved ( < 0.05). Collectively, PB supplementation protected the pigs against ETEC K88 infection by enhancing immune responses and attenuating intestinal damage and improved the performance and nutrient digestibility of weaned pigs. Therefore, PB could be a potential effective alternative to AB for ameliorating diarrhea and improving performance in weaned pigs.
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We investigated the effects of Forsythia suspensa extract (FSE) and chito-oligosaccharide (COS), alone or together, on performance and health status of weaned piglets. The treatments included a basal diet and three diets with 160 mg/kg COS, 100 mg/kg FSE, or 100 mg/kg FSE and 160 mg/kg COS. Supplementation with COS or FSE alone improved (P < 0.01) average daily gain and feed conversion ratio compared with the basal diet in the first 2 weeks. On day 14, COS or FSE supplementation separately produced stronger (P < 0.01) serum total antioxidant capacity and glutathione peroxidase activities and lower serum endotoxin (P < 0.05) and malondialdehyde (P < 0.01) concentrations, generated higher (P < 0.01) serum complement 4 concentration, peripheral blood lymphocyte proliferation and serum-specific ovalbumin antibody level than the basal diet. No differences in oxidative injury and immunity indices were detected on day 28. The combined FSE and COS produced similar results compared with FSE or COS when given alone. These data indicate FSE or COS can increase performance by modulating intestinal permeability, antioxidant status and immune function in younger pigs. There appears to be similar advantage in feeding the additives in combination over those obtained from feeding them separately.