Effects of mannan oligosaccharides on performance and microorganism fecal counts of calves following an enhanced-growth feeding program

Animal Feed Science and Technology 137 (2007) 115–125

Effects of mannan oligosaccharides on performance and microorganism fecal counts of calves following an enhanced-growth feeding program M. Terr´e a , M.A. Calvo c , C. Adelantado c , A. Kocher d , A. Bach a,b,∗ a

Grup de Recerca i Nutrici´o, Maneig i Benestar Animal, Universitat Aut`onoma de Barcelona, Unitat de Remugants-IRTA (Institut de Recerca i Tecnologia Agroaliment`aries), Barcelona 08193, Spain b Instituci´ o Catalana de Recerca i Estudis Avan¸cats (ICREA), Barcelona 08010, Spain c Departament de Sanitat i d’Anatomia Animals, Universitat Aut` onoma de Barcelona, Barcelona 08193, Spain d Alltech Biotechnology P/L, 68-70 Nissan Dr. Darndenong South, Vic. 3175, Australia Received 24 July 2006; received in revised form 28 September 2006; accepted 7 November 2006

Abstract Sixty female Holstein calves were used to study the effect of mannan oligosaccharides (MOS) on performance, health, bacteria fecal counts and Cryptosporidium presence in feces of calves following an enhanced-growth feeding program. Calves were divided in two groups: supplementation of 4 g/d of MOS on milk replacer (MR-M) or non-supplemented milk replacer (MR-C). After 1 wk of adaptation to milk replacer (MR) at 180 g/kg dilution, calves were fed: 4 l/d of MR from 1 to 7 d, 6 l/d from 8 to 14 d, 7 l/d from 15 to 21 d, 6 l/d from 22 to 28 d, and 3 l/d once daily in the afternoon meal from 29 to 34 d. Calves were weaned at 35 d of study, and were offered water and starter ad libitum until 41 d of

Abbreviations: ADG, average daily gain; BW, body weight; CP, crude protein; DM, dry matter; MOS, mannan oligosaccharides; MR, milk replacer; MR-M, milk replacer supplemented with mannan oligosaccharides; MR-C, control milk replacer ∗ Corresponding author at: Grup de Recerca i Nutrici´ o, Maneig i Benestar Animal, Universitat Aut`onoma de Barcelona, Unitat de Remugants-IRTA (Institut de Recerca i Tecnologia Agroaliment`aries), Barcelona 08193, Spain. Tel.: +34 935 910 127; fax: +34 935 863 122. E-mail address: [email protected] (A. Bach). 0377-8401/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.anifeedsci.2006.11.009

116

M. Terr´e et al. / Animal Feed Science and Technology 137 (2007) 115–125

study. Starter and MR intake were recorded daily. Calves were weighed weekly, and blood samples were obtained at 1, 3, 5 and 6 wk of study to determine haptoglobin serum concentrations. Moreover, total fecal counts of Clostridium perfringens and Escherichia coli, and for presence of Salmonella spp. and Cryptosporidium spp. were determined from fecal samples obtained at 1, 2, and 3 wk of study. There were no differences in body weight, but starter intake tended to be greater (P=0.09) during the pre-weaning period (0.34 versus 0.28 ± 0.023 kg/d) and greater (P<0.01) the week after weaning (1.94 versus 1.71 ± 0.044 kg/d) in MR-M compared with MR-C calves. However, there were no differences in average daily gain between treatments during the pre-weaning (0.91 versus 0.90 ± 0.017 kg/d), and the post-weaning period (1.20 versus 1.22 ± 0.074 kg/d) between MR-C and MR-M, respectively. Consequently, the gain to feed ratio was lower (P<0.05) during the pre-weaning period (0.70 versus 0.74 ± 0.010), and tended to be lower during the post-weaning period (0.59 versus 0.66 ± 0.033) in MR-M than in MR-C treatment. Serum haptoglobin concentration was similar in both treatments. There were no differences in E. coli fecal counts between treatments. Calves in the MR-M treatment had lower Cryptosporidium spp. presence in feces during the first wk of study (P<0.05), but there were no differences thereafter. The supplementation of MOS in the MR stimulated starter intake after weaning, but this supplementation did not show a determining effect on reducing bacteria counts or Cryptosporidium spp. presence in calf feces, nor in rate of growth. © 2006 Elsevier B.V. All rights reserved. Keywords: Mannan oligosaccharides; Enhanced-growth; Dairy calves

1. Introduction The use of antibiotics in milk replacer (MR) of calves has been a common practice in animal production to improve feed efficiency and prevent diseases, especially scours during the first wk of calves life. However, the overuse of antibiotics exerts selective pressure that renders antibiotics ineffective (Amabile-Cuevas et al., 1995), and EU banned the use of antibiotics as growth promoters in animal nutrition (1831/2003 EEC). Several additives have been proposed to improve calf health as alternatives to the use of antibiotics as growth promoters. Mannan oligosaccharides (MOS) are complex mannose sugars derived from cell wall fragments of yeast that are believed to block the colonization of digestive pathogens increasing the competition for attachment sites in the digestive tract (Heinrichs et al., 2003). When MR was supplemented with antibiotics or MOS, a reduction in calf scours was observed compared with control (no additives) treatment (Heinrichs et al., 2003). Furthermore, feeding fructo ologosaccharides in combination to spray-dried bovine serum to calves reduced the incidence and severity of enteric disease (Quigley et al., 2002). However, MOS supplementation in the MR or concentrates have shown inconsistent results. Calves fed MR with 4 g/d of MOS increased starter intake, but this increase did not result in growth differences (Heinrichs et al., 2003). Contrarily, calves receiving a combination of probiotics, allicin, and fructoologosaccharides resulted in equivalent performance than calves that received antibiotics during the first 5 wk of life (Donovan et al., 2002). Although MOS have been reported to alter lymphocyte response in vitro (Muchmore et al., 1990), its effects on animal immune system are not well established. In recent years, enhanced-growth feeding programs for dairy calves have been proposed to increase growth rate during the pre-weaning period (Brown et al., 2003; Shamay et al., 2005). Feeding high

M. Terr´e et al. / Animal Feed Science and Technology 137 (2007) 115–125

117

amounts of milk replacer (Diaz et al., 2001; Jasper and Weary, 2002) resulted in increased fecal consistency. Thus, the use of MOS could help to palliate any negative effects of increasing fecal consistency, avoiding the colonization of digestive pathogens, and improve feed efficiency of milk replacer. The objective of this study was to evaluate the effect of MOS supplementation in the milk replacer of calves reared using an enhanced-growth feeding program on growth performance and microorganism counts in feces.

2. Materials and methods 2.1. Animals and treatments Sixty female Holstein calves (weighing 43.7 ± 4.55 kg and aging 9.8 ± 4.19 d) arrived from different farms to a commercial contract-heifer operation (Rancho Las Nieves, Mall´en, Spain) under the approval and supervision of the Animal Care Committee of IRTA. Upon arrival, they were weighed and allocated to individual pens (1.07 × 1.60 m). Then, calves were randomly distributed in two groups: calves following an enhanced-growth feeding program with MOS supplementation (4 g/d of Bio-Mos® , MR-M) or calves following an enhanced-growth feeding program without any supplementation (MR-C). Bio-MOS® is a natural product derived from the outer cell wall of a specific strain of Saccharomyces cerevisiae using a proprietary process developed by the manufacturer (Alltech Inc., Nicholasville, KY). The product contains mannan, glucan, protein, and various other components found in the yeast cell wall (100% purity). The quality and consistency of the product was tested by the manufacturer using a specific biological test (agglutination rate coefficient) as mentioned by Newman (2006). The first wk of study was considered an adaptation period, and calves received 4 l/d of MR at 120 g/kg dilution during the first 3 d, and 4 l/d at 150 g/kg dilution during the last 4 d of the adaptation week. After that, calves received the same MR (250 g CP/kg dry matter and 192 g fat/kg dry matter, Sprayfo Excellent 60, Sloten BV, Holland) diluted to obtain 180 g/kg dilution (Table 1). Milk replacer was offered with feeding bottles twice daily at 0700 and 1700. Calves received 4 l/d of MR from 1 to 7 d, 6 l/d from 8 to 14 d, 7 l/d from 15 to 21 d, 6 l/d from 22 to 28 d, and 3 l/d once daily in the afternoon meal from 29 to 34 d. Calf starter (Table 1) and water were offered ad libitum throughout the study. All calves were weaned at 35 d from the Table 1 Chemical composition of milk replacer and starter

Nutrient composition (g/kg DM) Crude protein Ether extract Neutral detergent fiber Acid detergent fiber Ash Gross energy (MJ/kg DM)

Milk replacer

Starter

249.5 191.6 1.5 – 64.3 21.7

196.6 37.8 187.3 81.7 68.5 18.7

118

M. Terr´e et al. / Animal Feed Science and Technology 137 (2007) 115–125

beginning of the study, and calf starter was offered until day 41 of the study. Animals were vaccinated against Clostridium perfringens (type B, C, D), Clostridium septicum, Clostridium novyi, Clostridium tetani, Clostridium sordellii, Clostridium chauvoei with Miloxan (Merial, Lyon, France), and bovine respiratory syncytial virus (BRSV), Parainfluenza-3 virus, Pasteurella haemolytica with Bovipast RSP (Intervet, Boxmeer, Holland) at 23 d of age and were revaccinated 3 wk later. 2.2. Measurements and sample collection The MR and starter intake were measured daily. Body weight was measured once weekly. Scour scores were recorded daily during the pre-weaning period following the scale (1: firm, not hard; 2: soft; 3: runny; and 4: watery) proposed by Larson et al. (1977). All medical treatments applied were recorded throughout the study. Between 2 and 4 h after the morning offer, 10 ml of blood were collected from the same 18 randomly selected calves of each treatment by venipuncture of the jugular vein into an evacuated blood collection tube at 1, 3, 5 and 6 wk of study. Blood was kept cold in ice and centrifuged at 1500 × g for 15 min to obtain serum. Serum samples were stored at −20 ◦ C until subsequent determination of haptoglobin. Feces were collected at 1, 2, and 3 wk of study and stored in the refrigerator until subsequent determination of total count of Escherichia coli, Salmonella spp., C. perfringens and Cryptosporidium spp. To determine E. coli, 1 ml of fecal samples diluted at 1:10, 1:100 and 1:1000 was inoculated in tubes containing inverted D¨urham tubes with 10 ml of McConkey agar and incubated at 31 ◦ C for 48 h. Presence of E. coli was positive when gas is present at least in 1/10 of the inverted D¨urham tubes. A second incubation was performed with the positive samples in 10 ml of brilliant green bile lactose (BGBL) broth with D¨urham tubes at 42 and at 31 ◦ C. Positive tubes were confirmed streaking the samples on a MacConkey agar. When gas production was positive in the BGBL broth at 42 ◦ C and E. coli was present in the MacConkey agar, E. coli was quantified per gram of sample. To determine Salmonella spp. in feces, 25 g of each fecal sample was enriched in a lactose broth and incubated at 37 ◦ C for 18 h. After that, an aliquote was spread in a selenite–cystin broth and incubated at 37 ◦ C for 24 h. Finally, from the broth obtained, samples were spread in two differential cultures: SS agar and phenol red brilliant green agar, and incubated at 37 ◦ C for 48 h. Several dilutions of fecal samples were performed to analyze C. perfringens. After that, 1 ml of each sample was incubated in an anaerobe stove at 42 ◦ C for 48 h in SPS agar with a paraffin slide on the top of the tube. Finally, black colonies were quantified according to the initial dilution. Fecal Cryptosporidium spp. presence was determined following the formalin–ethyl acetate sedimentation method and smears of the sediment were stained by the modified Ziehl–Nielsen technique (Henriksen and Pohlez, 1981). 2.3. Chemical analyses Samples of MR and starter were analyzed for dry matter (DM) (24 h at 103 ◦ C), ash (4 h at 550 ◦ C), N content using the AOAC (1990) method (988.05) adapted for an automatic distiller Kjeldhal (Kjeltec Auto 1030 Analyzer, Tecator, Sweden) and using CuSO4 /Se as catalyst instead of CuSO4 /TiO2 , ether extract using the AOAC method (920.39) using petroleum ether for distillation instead of diethyl ether (AOAC, 1990), neutral detergent

M. Terr´e et al. / Animal Feed Science and Technology 137 (2007) 115–125

119

fiber assayed with heat stable amylase and expressed including residual ash, acid detergent fiber expressed inclusive residual ash (van Soest et al., 1991), and gross energy with an adiabatic calorimeter (IKA-calorimeter C 4000, Heitersheim, Germany). 2.4. Statistical analyses Performance, haptoglobin serum concentrations, and Salmonella spp., E. coli, and C. perfringens total counts were analyzed with an analysis of variance with repeated measures. The statistical model included calf as a random effect, and MOS supplementation, time, and their interaction as fixed effects. The initial body weight (BW) and age were used as a covariate for measures of the pre-weaning period, and BW and age at weaning for measures of the post-weaning period. The model for each dependent variable (Y) was as follows: Yijklm = μ + calfi + BWj + agek + MOSl + timem + (MOS × time)lm + εijklm where μ represents the overall mean, calf the random effect of calf j, BWi and agej the covariates, MOSk the treatment effect, timel the day of study, and εijklm represents the random error. Statistical significance was considered to exist for P≤0.05. Due to the lack of normality, serum haptoglobin concentration was transformed to a natural logarithm, and data from bacteria total count were transformed to log10 before analyses were conducted. The means for haptoglobin concentrations presented herein correspond to non-transformed data, and SE and P-values correspond to the analysis of variance using log-transformed data. Fecal scores were grouped in two categories: score of 1 and 2 were considered a single category illustrating absence of loose feces, and scores of 3 and 4 were grouped into another single category representing presence of loose feces. Due to the low incidence of loose feces the analysis was performed considering absence of loose feces within a week (0), presence of loose feces, at least, once within a week (1). The incidence of medical and oral rehydratant treatments were analyzed as the number of medical or oral rehydratant treatment within each week for each calf. Both data (feces and medical treatments) were analyzed with a mixedeffects logistic regression model using calf as a random effect and MOS supplementation and time as fixed effects. Similarly, the probability for observing Cryptosporidium spp. in feces was analyzed using a mixed-effects logistic regression with calf as a random effect, and week, MOS supplementation, and their interaction as fixed effects.

3. Results and discussion 3.1. Performance Body weight was similar between treatments throughout the study (Table 2). Average daily gain was similar between both treatments, but tended (P=0.05) to evolve differently during the pre-weaning period. Calves in MR-M treatment increased average daily gain (ADG) from 14 to 21 d, in contrast to MR-C calves that maintained the same ADG during this period, but afterwards both treatments presented the same ADG pattern. Milk replacer DM intake was similar between treatments but evolved differently (P<0.05) over time (Fig. 1). Calves in MR-M treatment presented greater MR intake during the 9th and 10th d of

120

M. Terr´e et al. / Animal Feed Science and Technology 137 (2007) 115–125

Table 2 Least square means of performance parameters and intake of calves following an enhanced-growth feeding program without (MR-C) or with (MR-M) mannan oligosaccharides supplementation during the pre- and post-weaning periods Item

MR supplementationa

SEb

MR-C

MR-M

Pre-weaning, 1–34 d Initial BW (kg) ADG (kg/d) DMI of MR (kg/d) DMI of starter (kg/d) Gain:feed ratio

44.7 0.91 0.94 0.28 0.74

45.5 0.90 0.95 0.34 0.70

1.05 0.017 0.001 0.023 0.010

Post-weaning, 35–41 d Final BW (kg) ADG (kg/d) DMI of starter (kg/d) Gain:feed ratio

84.5 1.20 1.71 0.66

85.3 1.22 1.94 0.59

1.42 0.074 0.044 0.033

P-valuec T

MO × T

0.91 0.66 0.49 0.09 0.02

<0.001 <0.001 <0.001 <0.001 <0.001

0.17 0.05 0.04 0.57 0.11

0.68 0.85 <0.001 0.09

– – <0.001 –

– – 0.06 –

MO

a MR-C: enhanced-growth feeding program; MR-M: enhanced-growth feeding program supplemented with mannan oligosaccharides. b SE: standard error of the mean. c MO: effect of mannan oligosaccharide supplementation; T: time effect; MO × T: effect of the interaction between mannan oligosaccharide supplementation and time.

Fig. 1. Milk replacer dry matter intake in calves supplemented with (open bars) or without (closed bars) mannan oligosaccharides in the milk replacer from day 8 until day 28 of study.

M. Terr´e et al. / Animal Feed Science and Technology 137 (2007) 115–125

121

Fig. 2. Starter dry matter intake in calves supplemented with (䊉) or without () mannan oligosaccharides in the milk replacer throughout the study. The arrow points the weaning day.

study compared with MR-C calves, coinciding with the start of the 6 l/d offer. Furthermore, starter DM intake tended to be greater (P=0.09) during the pre-weaning period and greater (P<0.01) during the post-weaning period in MR-M compared with MR-C calves (Fig. 2). Moreover, calves supplemented with MOS tended (P=0.06) to increase their starter DM intake more vigorously after weaning. Due to the differences in starter and MR intakes during the pre-weaning period and the similar ADG in MR-M and MR-C treatments, the gain to feed ratio was lower (P<0.05) in MR-M compared with MR-C calves during the pre-weaning period (Table 2). In the present study, starter DM intake tended to be different (P=0.09) during the pre-weaning period, in contrast to Donovan et al. (2002) who reported no differences in grain intake when MR was offered. However, similar to the present study, calves weaned at 5 wk of age and fed MR supplemented with MOS consumed more grain the week after weaning than calves supplemented with antibiotic in the MR (Heinrichs et al., 2003). However, chickens receiving diets supplemented with different levels of MOS did not present differences in feed intake and weight gain (Iji et al., 2001), although weanling pigs fed a diet with MOS improved their performance when antibiotics were also included in the diet, suggesting that the use of antibiotics might result in a favorable gut microflora for a positive MOS response (LeMieux et al., 2003). 3.2. Fecal score and medical treatments There were no differences in the incidence of loose feces between MR-C and MR-M treatments. Furthermore, there were no differences in number of days on medical or oral

122

M. Terr´e et al. / Animal Feed Science and Technology 137 (2007) 115–125

rehydratant treatment in MR-C and MR-M calves throughout the study. Similar to our study, calves supplemented with MOS or with a mix of additives, containing fructooligosaccharides, presented similar fecal scores and frequency of oral electrolyte therapy than calves supplemented with antibiotics (Donovan et al., 2002; Heinrichs et al., 2003). However, Heinrichs et al. (2003) reported that calves receiving MR supplemented with MOS or antibiotics had a greater probability of having normal feces than non-supplemented calves. In our study, the incidence of pathology was low, and potential MOS benefits on health might have been evident if calves had been challenged with a disease or some other powerful stressors, as reported in the study by Fairchild et al. (2001) who found a BW improvement in poultry challenged with E. coli and supplemented with MOS. 3.3. Fecal counts All fecal samples were negative to the presence of Salmonella spp. Moreover, there were no differences between treatments in E. coli or C. perfringens fecal quantification (Table 3) during 1, 2 and 3 wk of study. Similar results have been reported where the inclusion of MOS in a poultry diet did not reduce the total number of coliform in the ceca (Fairchild et al., 2001). However, E. coli counts increased (P<0.02) in feces in calves from 2 to 3 wk of study in both treatments, but similar counts were found in C. perfringens samples throughout the first 3 wk of study (Table 3). This lack of differences in Clostridium counts between treatments across time might have been expected as all calves were vaccinated against Clostridium at 23 d of age, and revaccinated 3 wk later, although vaccination success rate is variable (Troxel et al., 1997). Overall, the probability of observing presence (% of positive samples) of Cryptosporidium spp. in the fecal smear preparations of calf feces was numerically lower in MR-M calves (P=0.16) compared with MR-C calves (0.23 versus 0.35, respectively). However, the probability of observing presence of Cryptosporidium spp. in feces evolved differently (P=0.01) between treatments over time. Calves in MR-C treatment had the greatest probability of showing Cryptosporidium spp. the first wk of the study, and decreased during the second and third wk of study, in contrast to MR-M calves that presented a low probability of showing of Cryptosporidium spp. throughout the first 3 wk of the study (Fig. 3). Table 3 Least squares means of total fecal counts (log10 cfu/g of feces) of Escherichia coli and Clostridium perfringens throughout the first 3 wk of study of calves following an enhanced-growth feeding program supplemented with (MR-M) or without (MR-C) mannan oligosaccharides in the milk replacer SEa

Week of study 1

2

3

MR-C E. coli C. perfringens a

7.03 4.51

1

2

3

7.06 3.82

7.18 4.22

P-valueb MO

T

MO × T

0.54 0.49

0.02 0.23

0.32 0.28

MR-M 6.87 4.08

7.29 3.95

7.13 4.12

0.070 0.131

SE: standard error of the mean. MO: effect of mannan oligosaccharide supplementation; T: time effect; MO × T: effect of the interaction between mannan oligosaccharide supplementation and time. b

M. Terr´e et al. / Animal Feed Science and Technology 137 (2007) 115–125

123

Fig. 3. Probability of observing Cryptosporidium spp. in calves feces during the first 3 wk of the study. Calves supplemented with (MR-M, ) or without (MR-C, ) mannan oligosaccharides in the milk replacer throughout the study.

The differences between the two treatments in the appearance of Cryptosporidium spp. in feces the first wk of the study may be influenced by management practices in the origin farms (J¨ager et al., 2005) or initial IgG against Cryptosporidium spp. (Teunis et al., 2002). However, the number of calves in the current study might have not sufficient to determine if MOS has a direct effect on Cryptosporidium presence in feces. The mode of action of MOS in preventing bacteria attachment to the intestinal wall is by blocking lectins of the bacteria cell wall that bind to receptors containing d-mannose in the gastrointestinal tract (Spring et al., 2000), such as the mannose-specific lectins of type-1 fimbriae of E. coli (Friman et al., 1996). On the other hand, Cryptosporidium spp. presents N-acetyl-dgalactosamide and the N-acetyl-d-glucosamide c-specific lectins as surface carbohydrates that may play a role in the pathogenesis of cryptosporidiasis (Llovo et al., 1993). More recently, it was observed that galactose-N-acetylgalactosamide epitopes of glycoproteins on the apical membranes of intestinal epithelia and sporozoites surface were also involved in Cryptosporidium spp. attachment to the intestinal epithelial cells (Chen and Larusso, 2000). Further research is needed to determine whether MOS supplementation may reduce the presence of Cryptosporidium spp. in feces by attaching to its sugar-specific lectins. 3.4. Serum haptoglobin There were no differences in serum haptoglobin concentrations between treatments (0.17 versus 0.17 ± 0.029 mg/ml, in MR-C and MR-M treatments, respectively). Haptoglobin

124

M. Terr´e et al. / Animal Feed Science and Technology 137 (2007) 115–125

is an acute phase protein that undergoes substantial quantitative changes in response to infection, inflammation, or trauma (Heinrich et al., 1990). Mannan oligosaccharides may have an inhibitory effect on lymphocyte function (Muchmore et al., 1990). Thus, a decrease in serum haptoglobin concentrations as a result of the vaccination was expected but not observed in the current study. Unexpected results were also found in pigs supplemented with MOS and challenged with Salmonella spp. oral infection that slightly increased haptoglobin serum concentrations after the challenge (Burkey et al., 2004). 4. Conclusions The supplementation of mannan oligosaccharides in the MR stimulated starter intake after weaning without further consequences in growth rate leading to a lower feed efficiency, and did not show a determining effect on reducing fecal bacteria counts or Cryptosporidium spp. presence in feces. Acknowledgments The authors thank Alltech for the financial support and Rancho Las Nieves for allowing the development of this study in their facilities. The authors express a special thanks to Pepe, Jos´e Lu´ıs, Carolina, Fernando, and Bernat from Rancho Las Nieves. The authors thank INIA (Instituto Nacional de Investigaciones Agrarias) for the fellowship that supported the work of Marta Terr´e. References Amabile-Cuevas, C., Cardenas-Garc´ıa, M., Ludgar, M., 1995. Antibiotic resistance. Am. Sci. 83, 320–329. Association of Official Analytical Chemists, 1990. Official Methods of Analysis, 15th ed. AOAC, Arlington, VA. Brown, E.G., VandeHaar, M.J., Daniels, K.M., Liesman, J.S., Chapin, L.T., Keisler, D.H., Weber Nielsen, M.S., 2003. Effect of increasing energy and protein intake on body growth and carcass composition of heifer calves. J. Dairy Sci. 88, 585–594. Burkey, T.E., Dritz, S.S., Nietfeld, J.C., Johnson, B.J., Minton, J.E., 2004. Effect of dietary mannan oligosaccharide and sodium chlorate on the growth performance, acute-phase response, and bacterial shedding of weaned pigs challenged with Salmonella enterica serotype Typhimurium. J. Anim. Sci. 82, 397–404. Chen, X., Larusso, N.F., 2000. Mechanism of attachment and internalization of Cryptosporidium parvum to biliary and intestinal epithelial cells. Gastroenterology 118, 368–379. Diaz, M.C., Van Amburgh, M.E., Smith, J.M., Kelsey, J.M., Hutten, E.L., 2001. Composition of growth of Holstein calves fed milk replacer from birth to 105-kilogram body weight. J. Dairy Sci. 84, 830–842. Donovan, D.C., Franklin, S.T., Chase, C.C.L., Hippen, A.R., 2002. Growth and health of Holstein calves fed milk replacers supplemented with antibiotics or enteroguard. J. Dairy Sci. 85, 947–950. Fairchild, A.S., Grimes, J.L., Jones, F.T., Wineland, M.J., Edens, F.W., Sefton, A.E., 2001. Effects of hen, Bio-Mos® , and Flavomycin® on poult susceptibility to oral Escherichia coli challenge. Poult. Sci. 80, 562–571. Friman, V., Adlerberth, I., Connell, H., Svanborg, C., Hanson, L.A., Wold, A.E., 1996. Decreased expression of mannose-specific adhesins by Escherichia coli in colonic microflora of immunoglobulin A-deficient individuals. Infect. Immum. 64, 2794–2798. Heinrich, P.C., Castell, J.V., Andus, T., 1990. Interleukin-6 and the acute phase response. Biochem. J. 265, 621–636.

M. Terr´e et al. / Animal Feed Science and Technology 137 (2007) 115–125

125

Heinrichs, A.J., Jones, C.M., Heinrichs, B.S., 2003. Effects of mannan oligosaccharide or antibiotics in neonatal diets on health and growth of dairy calves. J. Dairy Sci. 86, 4064–4069. Henriksen, S.A., Pohlez, J.F.L., 1981. Staining of cryptosporidia by a modified Ziehl–Nielsen technique. Acta Vet. Scand. 22, 594–596. Iji, P.A., Saki, A.A., Tivey, D.R., 2001. Intestinal structure and function of broiler chickens on diets supplemented with a mannan oligosaccharide. J. Sci. Food Agric. 81, 1186–1192. J¨ager, M., Gauly, M., Bauer, C., Failing, K., Erhardt, G., Zahner, H., 2005. Endoparasites in calves of beef cattle herds: management systems dependent and genetic influences. Vet. Parasitol. 131, 173–191. Jasper, J., Weary, D.M., 2002. Effects of ad libitum milk intake on dairy calves. J. Dairy Sci. 85, 3054–3058. Larson, L.L., Owen, F.G., Albright, J.L., Appleman, R.D., Lamb, R.C., Muller, L.D., 1977. Guidelines toward uniformity in measuring and reporting calf experimental data. J. Dairy Sci. 60, 989–991. LeMieux, F.M., Southern, L.L., Bidner, T.D., 2003. Effect of mannan oligosaccharides on growth performance of weanling pigs. J. Anim. Sci. 81, 2482–2487. Llovo, J., Lopez, A., Fabregas, J., Mu˜noz, A., 1993. Interaction of lectins with Cryptosporidium parvum. J. Infect. Dis. 167, 1477–1480. Muchmore, A.V., Sathyamoorthy, N., Decker, J., Sherblom, A.P., 1990. Evidence that specific high-mannose oligosaccharides can directly inhibit antigen-driven T-cell responses. J. Leukoc. Biol. 48, 457–464. Newman, K., 2006. Quantifying the efficacy of MOS. Feed Mix 14 (1), 2–4. Quigley III, J.D., Kost, C.J., Wolfe, T.A., 2002. Effects of spray-dried animal plasma in milk replacers or additives containing serum and oligosaccharides on growth and health of calves. J. Dairy Sci. 85, 413–421. Shamay, A., Werner, D., Moallem, U., Barash, H., Bruckental, I., 2005. Effect of nursing management and skeletal size at weaning on puberty, skeletal growth rate, and milk production during first lactation of dairy heifers. J. Dairy Sci. 88, 1460–1469. Spring, P., Wenk, C., Dawson, K.A., Newman, K.E., 2000. The effects of dietary mannan oligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca of Salmonella-challenged chicks. Poult. Sci. 79, 205–211. Teunis, P.F., Chappell, C.L., Okhuysen, P.C., 2002. Cryptosporidium dose–response studies: variation between hosts. Risk Anal. 22, 475–485. Troxel, T.R., Burke, G.L., Wallace, W.T., Keaton, L.W., McPeak, S.R., Smith, D., Nicholson, I., 1997. Clostridial vaccination efficacy on stimulating and maintaining an immune response in beef cows and calves. J. Anim. Sci. 75, 19–25. van Soest, P.J., Robertson, J.B., Lewis, B.A., 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583–3597.