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The effects of group size and subtherapeutic antibiotic alternatives on growth performance and morbidity of nursery pigs: a model for feed additive evaluation † † Kristin M. Olsen,* Nicholas K. Gabler,* Chris J. Rademacher, Kent J. Schwartz, ‡ ,2 Wesley P. Schweer,* Gene G. Gourley, and John F. Patience* *Department of Animal Science, Iowa State University, Ames, IA 50011; Department of Veterinary Diagnostic and Production Animal Medicine, Iowa State University, Ames, IA 50011; and Gourley Research Group, Webster City, IA 50595 ABSTRACT: The objectives of this experiment were used to characterize health status. Pigs experienced to evaluate the effects of alternatives to antibiotic natural challenges of acute diarrhea and septicemia growth promoters (AGP), two group sizes, and their in week 1 and porcine reproductive and respiratory interaction on nursery pig performance to serve as syndrome virus (PRRSV) in weeks 4–6. There was a model for future AGP alternative studies. A 41-d a significant interaction between diet and group size experiment was conducted in a commercial wean- for ADG (P = 0.012). PC increased ADG in large to-finish barn; 1,300 piglets weaned at 21 d of age and small groups (P < 0.05) and ZA increased ADG (weaned 2 or 4 d prior to experiment; 6.14 ± 0.18 kg only in large groups (P < 0.05). Small groups had BW; PIC 1050 sows and multiple sire lines) were improved ADG compared to large groups when fed blocked by sire, sex, and weaning date, then assigned NC or DR diets (P < 0.05). Similarly, PC increased to eight treatments: four dietary treatments each ADFI (P < 0.05). Compared to NC, ZA improved evaluated across two group sizes. The four dietary ADFI in large groups only (P < 0.05; diet × group treatments were: negative control (NC), positive con- size: P = 0.015). Pigs fed PC had greater G:F than NC trol (PC; NC + in-feed antibiotics), zinc oxide plus (P < 0.05), and small groups had greater G:F than a dietary acidifier (blend of fumaric, citric, lactic, large groups (P < 0.05). There was no effect of ZA and phosphoric acid) (ZA; NC + ZnO + acid), and or DR on G:F. Pigs fed PC required fewer individual a Bacillus-based direct-fed-microbial (DFM) plus medical treatments than NC and pigs fed ZA were resistant potato starch (RS) (DR; NC + DFM + RS). intermediate (P = 0.024). More pigs were removed The two group sizes were 31 or 11 pigs/pen; floor from large than small groups (P = 0.049), and there space was modified so area/pig was equal between the was no effect of diet on removals (P > 0.10). In con- group sizes (0.42 m /pig). There were 7 pens/diet with clusion, careful study design, protocol implementa- 11 pigs/pen and 8 pens/diet with 31 pigs/pen. Data tion, sample collection, and recording of important were analyzed as a randomized complete block design information allowed us to characterize the health with pen as the experimental unit. Diagnostic assess- status of this group of pigs and determine treatment ment of oral fluids, serum, and tissue samples was effects on growth performance and morbidity. Key words: antibiotic growth promoter, pen size, porcine reproductive and respiratory syndrome virus, swine © The Author(s) 2018. Published by Oxford University Press on behalf of the American Society of Animal Science. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-com- mercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact firstname.lastname@example.org Transl. Anim. Sci. 2018.2:298–310 The authors would like to thank the National Pork doi: 10.1093/tas/txy068 Board, Des Moines, IA, for financial support of this research. Corresponding author: email@example.com Received May 1, 2018. Accepted June 26, 2018. Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 Evaluation of antibiotic alternatives 299 INTRODUCTION Animals, Housing, and Management Consumer interest in pork raised without anti- One room of a commercial wean-to-finish biotics or with limited antibiotics and the intro- research barn was populated with 1,300 barrows and duction of the Veterinary Feed Directive in the gilts (6.14 ± 0.18 kg BW) derived from PIC 1,050 United States have encouraged producers to look females and four different sire lines (PIC Duroc, DNA for alternatives to antibiotic growth promoters Genetics Duroc, Genesus Duroc or PIC Pietrain) for (AGP) in feed. There are many products already a 42-d nursery study. The pigs were selected from a available that may be considered alternatives to study evaluating sire lines, thus explaining the larger AGP. However, the efficacy of AGP alternatives in than normal number of sires represented in the experi- commercial pork production has not been clearly ment. All pigs used in the experiment came from the defined, and the results of AGP alternative stud - same sow source and were weaned at 21 d of age. On ies are often inconsistent (Jacela et al., 2009, 2010; day 1 after birth, all pigs were given iron and gen- Thacker, 2013; Liao and Nyachoti, 2017). This tamicin injections. Before weaning, pigs were treated may be due to inconsistent experiment methodol- on an individual basis with injectable antibiotics ogy, including differences in health status, genet- (gentamicin, ceftiofur, or enrofloxacin) as needed. At ics, experimental conditions, and diet composition weaning, pigs were vaccinated for porcine circovirus (Allen et al., 2013). This leaves a significant gap in type 2 and Mycoplasma hyopneumoniae (Circumvent knowledge about the effectiveness of AGP alter- PCV-MG2, Merck Animal Health, Madison, NJ), natives and the ability to make comparisons or and ileitis (Porcilis Ileitis, Merck Animal Health). observe trends across studies. To most efficiently Due to the flow schedule at the sow source, approxi - identify useful AGP alternatives and apply them in mately half of the pigs were weaned 4 d prior to the production, it is necessary first to increase the con - start of the experiment and held at the sow farm while sistency with which studies evaluating AGP alter- the other half was weaned 2 d prior to the start of natives are conducted. Therefore, there is a need for the experiment. For the duration of the experiment, an example protocol with guidelines for AGP alter- pigs were housed in a tunnel-ventilated barn. Each native studies. pen was equipped with a 4-space automatic dry self- Most published studies evaluating AGP alterna- feeder and nipple water drinker, fully slatted concrete tives have been conducted in academic research set- oors fl , and metal rod penning and gates. Pigs were tings, which typically house fewer pigs per pen than given ad libitum access to feed and water for the dur- commercial production facilities. Because group size ation of the experiment. An automatic feeding system may impact pig performance, specifically in the nurs - (Big Dutchman, Holland, MI) was used to deliver a ery phase (Wolter et al., 2000), one may question specified amount of feed to each pen. Air temperature whether the results of such studies could be differ- in the room averaged 28.5 °C ± 1.4, 28.7 °C ± 1.2, ent in a commercial setting. Furthermore, inherent 27.1 °C ± 0.5, 24.5 °C ± 1.1, 25.8 °C ± 0.9, 26.5 °C ± environmental differences between academic research 2.2, in weeks 1–6, respectively. facilities and commercial pork production facilities create the need for more commercial-scale data. Experimental Design The objective of this experiment was to test the effects of two different group sizes and AGP alter- Experimental treatments were arranged in a native diets on nursery pig growth performance, in split-plot design with four dietary treatments eval- order to serve as a framework for future AGP alter- uated across two group sizes. The dietary treat- native studies. This objective was selected to encour- ments included a negative control (NC) with no age greater progress in assessing the scientific merit AGP, a positive control (PC) consisting of the NC of said studies as rapidly as possible and to facilitate diet with either chlortetracycline hydrochloride the comparison of experimental results across mul- (phase 1 and 3) or tiamulin hydrogen fumarate tiple studies. (phase 2) added at the expense of corn, alterna- tive diet 1 (ZA) consisting of the NC diet with MATERIALS AND METHODS zinc oxide (ZnO) plus a dietary acidifier (blend All experimental procedures were reviewed and of phosphoric, fumaric, citric, and lactic acids; approved by the Iowa State University Institutional Kem-Gest, Kemin, Des Moines, IA) added at the Animal Care and Use Committee (number 3-17- expense of corn, and alternative diet 2 (DR) con- 8465-S). The study was conducted in central Iowa sisting of the NC diet with a Bacillus-based direct- in April and May 2017. fed microbial (DFM; BioPlus 2B, Chr. Hansen, Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 300 Olsen et al. Hoersholm, Denmark) plus resistant potato starch focusing on evaluating specific products. The spe - (MSP[RS], MSP Starch Products Inc., Carberry, cific combinations were chosen based on results Manitoba, Canada) added at the expense of corn. from Schweer et al. (2017a) which indicated that Combinations of AGP alternatives were used, AGP alternatives in the categories of zinc/copper, rather than single products, to first help satisfy organic acids, and probiotics were most effective. the objective of testing a study design, rather than Furthermore, ZnO with an acidifier and a probiotic Table 1. Ingredient and nutrient composition of experimental diets (as fed basis): phase 1 and 2 Phase 1 Phase 2 Dietary treatment NC PC ZA DR NC PC ZA DR Ingredient, % Corn 34.24 33.94 33.64 29.19 52.80 52.62 52.40 47.75 Soybean meal 47% CP 17.50 17.50 17.50 17.50 27.50 27.50 27.50 27.50 Whey permeate 20.73 20.73 20.73 20.73 4.88 4.88 4.88 4.88 Dried yeast 11.12 11.12 11.12 11.12 3.56 3.56 3.56 3.56 Rolled oat groats 7.50 7.50 7.50 7.50 5.00 5.00 5.00 5.00 Choice white grease 3.48 3.48 3.48 3.48 3.48 3.48 3.48 3.48 Spray-dried plasma 3.00 3.00 3.00 3.00 — — — — Limestone 0.70 0.70 0.70 0.70 0.69 0.69 0.69 0.69 L-lysine HCl 0.51 0.51 0.51 0.51 0.48 0.48 0.48 0.48 MHA methionine 0.35 0.35 0.34 0.34 0.35 0.35 0.35 0.35 Monocalcium phosphate 0.31 0.31 0.31 0.31 0.54 0.54 0.54 0.54 VTM premix 0.18 0.18 0.18 0.18 0.18 0.18 0.18 0.18 Salt 0.15 0.15 0.15 0.15 0.28 0.28 0.28 0.28 Choline 0.12 0.12 0.12 0.12 0.12 0.12 0.12 0.12 L-Threonine 0.08 0.08 0.08 0.08 0.16 0.16 0.16 0.16 L-Tryptophan 0.03 0.03 0.03 0.03 — — — — CTC — 0.30 — — — — — — Tiamulin — — — — — 0.18 — — Zinc oxide — — 0.30 — — — 0.20 — Acidifier — — 0.30 — — — 0.20 — DFM — — — 0.05 — — — 0.05 Potato Starch — — — 5.00 — — — 5.00 Analyzed values Resistant starch, % — — — 1.89 — — — 1.82 DM% 89.0 88.8 89.0 88.8 87.6 87.7 87.3 87.3 Ether extract, % 5.60 5.96 6.04 5.76 6.06 6.45 6.13 6.14 Ca, % 0.68 0.72 0.64 0.72 0.59 0.61 0.57 0.61 P, % 0.61 0.62 0.63 0.60 0.51 0.53 0.51 0.52 Na, % 0.30 0.31 0.30 0.31 0.15 0.15 0.16 0.16 CP, % 21.00 21.60 20.40 21.00 19.60 19.80 19.10 19.00 Zinc, ppm 461 347 1900 459 432 357 1160 406 Phase 1 was fed from days 0 to 11, phase 2 was fed from days 12 to 24. Feed budget was 2.2 kg/pig for phase 1 and 5.4 kg/pig for phase 2. NC = negative control, PC = positive control: NC + dietary antibiotics, ZA = NC + ZnO + dietary acidifier, DR = NC + Bacillus-based direct- fed microbial + 5% resistant starch. VTM premix provided per kg of complete diet: 0.21 ppm Cr as Cr O , 10 ppm Cu as CuSO , and Cu-MHA chelate, 0.31 ppm I as calcium 2 3 4 iodate, 82 ppm Fe as FeSO , 21 ppm Mn as MnO and Mn-MHA chelate, 0.31 ppm Se as selenium yeast, 170 ppm Zn as ZnO and Zn-MHA chelate, 1,701 IU vitamin D3, 11,337 IU vitamin A, 45.3 IU vitamin E, 4.53 mg menadione, 0.23 mg biotin, 1.7 mg folic acid, 51 mg niacin, 15.6 mg pyridox- ine, 28.3 mg pantothenic acid, 8.5 mg riboflavin, 39.7 mg vitamin B12, 514.4 FTU phytase (AxtraPhy, Danisco Animal Nutrition, Marlborough, UK). Premix also contained per kg of complete diet 0.06 g of Bacillus-based direct-fed-microbial (1.6 × 10 CFU/g). CTC = chlortetracycline hydrochloride (Auromycin-100, Zoetis, Parsippany, NJ); Tiamulin hydrogen fumarate (Denagard 10, Elanco, Greenfield, IN). Blend of phosphoric, fumaric, citric, and lactic acids (Kem-Gest, Kemin, Des Moines, IA). 6 6 Bacillus spp. based direct-fed-microbial, provided 1.1 × 10 CFU/g of complete diet (BioPlus 2B, Chr. Hansen, Hoersholm, Denmark). Resistant potato starch (MSP[RS], MSP Starch Products Inc., Carberry, Manitoba, Canada). Diets with no value did not have high enough resistant starch content to be accurately measured by this assay. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 Evaluation of antibiotic alternatives 301 Table 2. Ingredient and nutrient composition of with a prebiotic likely have modes of action which experimental diets (as fed basis): phase 3 either compliment or do not antagonize each other. Diets were fed in three phases (Tables 1 and 2) Dietary Treatment based on a feed budgeting system. When a pen NC PC ZA DR consumed its entire allowance for a phase, feed for Ingredient, % the next phase was given to that pen. In this man- Corn 47.59 47.19 47.29 42.54 ner, all pens were allowed to consume their entire Soybean meal 46.5% CP 35.95 35.95 35.95 35.95 budget for each phase before moving to the next Corn DDGS 10.00 10.00 10.00 10.00 phase. In order to associate pig weights with phase Choice white grease 3.20 3.20 3.20 3.20 changes, weigh days were scheduled as close as Limestone 1.03 1.03 1.03 1.03 Lysine sulfate, 54.6% 0.67 0.67 0.67 0.67 possible to the first pens finishing their feed budget Monocalcium phosphate 0.54 0.54 0.54 0.54 from the previous phase. Phase 1 was fed from days Salt 0.46 0.46 0.46 0.46 0 to 11, phase 2 from days 12 to 24, and phase 3 DL-Methionine 0.19 0.19 0.19 0.19 from days 25 to 41.The first two phases were deliv - VTM premix 0.15 0.15 0.15 0.15 ered in pelleted form, and the third phase feed was L-Threonine 0.13 0.13 0.13 0.13 delivered as a mash. Feed was manufactured at two Vitamin E 0.05 0.05 0.05 0.05 different commercial feed mills (phases 1 and 2 at L-Tryptophan 0.04 0.04 0.04 0.04 the same mill, and phase 3 at another mill). Prior Phytase 0.01 0.01 0.01 0.01 to diet manufacturing, the acidifier, ZnO, DFM, CTC — 0.40 — — and RS products were hand-weighed on an ana- Zinc oxide — — 0.10 — lytical scale to the proper inclusion level, packaged Acidifier — — 0.20 — in individual bags, and delivered to the commercial DFM — — — 0.05 Potato starch — — — 5.00 mill. Mix sheets used during mixing from both feed Analyzed values mills were validated after mixing to ensure that Resistant starch, % — — — 3.90 these bags were added to the proper batches. In all DM, % 88.4 88.5 88.3 87.9 phases, the diet containing the DFM was mixed Ether extract, % 6.73 6.04 5.95 5.69 last in order to avoid contamination of the other Ca, % 0.67 0.75 0.71 0.68 three diets. P, % 0.60 0.61 0.60 0.58 Pigs were housed in groups of 31 (large groups; Na, % 0.21 0.26 0.22 0.21 Fig. 1) or 11 pigs each (small groups; Fig. 2). In CP, % 24.2 24.3 24.2 23.9 the small groups, a gate was installed to block off Zinc, ppm 138 196 701 240 approximately two-thirds of the pen to reduce usa- Phase 3 was fed from days 25 to 41. ble floor space; the two outer spaces of the feeders NC = negative control, PC = positive control: NC + dietary antibi- were blocked off to achieve approximately equal otics, ZA = NC+ ZnO + dietary acidifier, DR = NC + Bacillus-based feeder space per pig. Not counting the space occu- direct-fed microbial + 5% resistant starch. 3 pied by each feeder, large pens had 0.41 m per Vitamin–trace mineral premix provided per kg of complete diet: 11,013 IU of vitamin A, 1,651 IU of vitamin D, 33 IU of vitamin E pig, and small pens had 0.42 m per pig. Sixty pens (dl-alpha tocopheryl acetate), 11 IU of vitamin E (d-alpha tocopheryl were utilized for a total of 15 replicates of each diet acetate), 4.4 mg of vitamin K, 0.029 mg of vitamin B , 5.51 mg of (eight large groups and seven small groups each), riboflavin, 38.55 mg of niacin, 22.03 mg of pantothenic acid, 0.22 mg 32 replicates of large groups and 28 replicates of of biotin, 1.10 mg of folic acid, 0.88 mg of pyridoxine, 0.396 mg of Co as CoCO , 0.015 g of Cu as CuO or CuSO , 0.22 mg of I as ethylenedi- small groups. Pigs were assigned to blocks based 3 4 amine dihydroiodide (EDDI) or CaI , 0.15 g of Fe as FeSO , 0.031 g of 2 4 on weaning date, sire line, and sex. Pigs held for 4 Mn as MnO or MnSO , 0.31 mg of organic Se as selenium yeast, and d or 2 d post-weaning were balanced within block 0.15 g of Zn as ZnO or ZnSO . to account for the potential influence of days OptiPhos 2000 (Huvepharma Inc., Peachtree City, GA). Chloratetracycline hydrochloride (Chlormax 50, Alpharma, post-weaning. Since four different sire lines were Bridgewater Township, NJ). used, sire line was balanced within block. Mixed- Blend of lactic, citric, fumaric, and phosphoric acids (Kem-Gest, sex pens were used, and sex was balanced within Kemin, Des Moines, IA). block. A total of 8 blocks were used, and pens were 7 6 Bacillus spp. based direct-fed-microbial product, provided 1.1 × 10 assigned to experimental treatments so that each CFU/g of complete diet (BioPlus 2B, Chr. Hansen, Hoersholm, Denmark). combination of diet and group size was represented Resistant potato starch (MSP[RS], MSP Starch Products Inc., in each block. However, since there were only 60 Carberry, Manitoba, Canada). pens, one block had only four large groups and no Diets with no value did not have high enough resistant starch con- small groups. tent to be accurately measured by this assay. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 302 Olsen et al. Figure 1. Large pen configuration. Pens were stocked with 31 pigs Figure 2. Small pen configuration. Pens were stocked with 31 pigs (0.41 m per pig). (0.42 m per pig). Table 3. Results of diagnostic testing throughout serum samples, and necropsies of pigs that died experiment (days 0 to 41) were used to confirm or rule out exposure to specific pathogens (Table 3). All diagnostic tests, includ- 1 2 3 4 Day Pathogen Result Testing method ing necropsies, were conducted at the Veterinary 3 Salmonella (S. infantitis) Positive Liver culture Diagnostics Laboratory at Iowa State University in 3 Actinobacillus suis Positive Lung culture Ames, Iowa. If a sample was positive for a specific 3 Streptococcus suis Positive Lung culture pathogen, the whole barn was considered to have 11 Mycoplasma hyorhinis Positive Fibrin swab PCR 26 PRRSV Positive Oral fluid PCR exposure to that pathogen. 26 IAV Negative Oral fluid PCR Under the direction of a veterinarian, pigs 26 Streptococcus suis Positive Lung culture were individually treated throughout the study with 26 Haemophilus parasuis Positive Lung culture injectable antibiotics (ceftiofur or enrofloxacin) for 40 PEDV Negative Oral fluid PCR and symptoms of lethargy, gauntness, severe diarrhea, serology coughing, or other signs of illness. Flunixamine was 40 PDCoV Negative Oral fluid PCR also given for a small number of cases of coughing 40 Mycoplasma Negative Oral fluid PCR and and labored breathing. Individual medical treat- hyopneumoniae serology ments were recorded daily by pen to determine if Day of sample collection. diet and group size influenced the number of treat - PRRSV = porcine reproductive and respiratory syndrome virus, ments required. Pigs were removed from the study IAV = influenza A virus, PEDV = porcine epidemic diarrhea virus, and housed in a hospital pen if they were injured, PDCoV = porcine deltacoronovirus. Samples were collected at necropsy from pigs that died as deter- extremely ill, or did not improve after treatment. mined necessary by the diagnostic veterinarian. On day 26, oral fluid The daily number of pigs removed was recorded samples from four symptomatic pens were collected and tested. On by pen. Pigs found dead were also recorded and day 40, oral fluid and serum samples from eight pens, equidistantly included in the daily removal records. spaced throughout the barn, were collected and tested. If a sample was positive for a specific pathogen, the whole barn was considered to have Oral fluid samples were collected via rope sam - exposure to that pathogen. pling from two pens per dietary treatment (eight PCR = polymerase chain reaction. pens total) on days 0, 21, and 40. Pens were cho- sen for oral fluid collection based on fixed special Characterization of Health Status sampling, so that each area of the barn was equally represented (Rotolo et al., 2017). A cotton rope was The pigs originated from a sow source that was hung in the pen for approximately 1 h, and fluid was negative for porcine reproductive and respiratory extracted from the rope by placing the saturated syndrome virus (PRRSV; confirmed through nega - end into a plastic bag and squeezing out the fluid tive oral fluid and serum PCR analysis). Oral fluids, (Prickett et al., 2008). The resulting fluid samples Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 Evaluation of antibiotic alternatives 303 were transferred to a plastic tube and stored at Growth Performance Data Collection −20 °C until analysis. Oral fluid samples were ana - Pigs were weighed by pen on a oor fl scale (val - lyzed using polymerase chain reaction (PCR) for idated with a standard check weight at each use) PRRSV, Influenza type-A virus of swine ( IAV-S), at the beginning and end of the experiment, and porcine epidemic diarrhea virus (PEDV), porcine at the end of each feed phase (days 11 and 24) to deltacoronovirus (PDCoV), and M. hyopneumo- determine ADG. Feed offered was weighed by the niae. Oral fluid samples were also collected from automatic feed delivery system, and remaining feed four pens exhibiting clinical symptoms (cough- was weighed at the end of each phase to determine ing, sneezing, lethargy) and tested for PRRSV and ADFI and G:F, measured as total BW gain:total IAV-S on day 26. Blood samples were collected from feed intake. Pen, removal date, BW at removal, and one pig per pen in two pens per dietary treatment reason for removal were recorded for each pig found (using the same pens as oral fluid collections) for a dead or removed from the study. This information total of eight blood samples on days 1 and 28. At was used to calculate pig days for each phase and the end of the trial (day 41), eight pigs per dietary the overall experimental period. treatment (one pig from each of the large pens) were euthanized for a separate experiment and blood was Calculations and Statistical Analysis collected from each. Ten milliliters of blood were collected by jugular venipuncture and centrifuged at The total number of medical treatments per 2,000 × g for 10 min at 4 °C, and the resulting serum pen was calculated as a proportion by dividing the was stored at −80 °C for later analysis. Serum sam- total number of treatments given for the whole ples from day 41 were tested for PEDV and M. hyo- experimental period by the number of pigs placed pneumoniae using PCR. The goal of this diagnostic in the pen (either 31 or 11). The proportion of total testing was to establish a general knowledge of dis- removals per pen was calculated by dividing the ease exposure and health status of the pigs used in total number of pigs removed for the whole period the study. in each pen by the number of pigs placed in the pen (either 31 or 11). Pig days were used to calculate Diet Sample Analysis ADG, ADFI, and G:F. The UNIVARIATE procedure of SAS (SAS Feed samples were taken directly from the feed- Inst. Inc. Cary, NC) was used to determine homo- ers of eight pens per dietary treatment during the geneity of variances and to identify outliers. middle of each feeding phase. To obtain each sam- Observations were considered outliers if greater ple, the feed in each feeder was stirred to assist in than three SD from the mean. Residual plots were homogeneity, and an approximately 200 g sample also used to verify equality of variances and nor- was taken by hand. All eight samples for each diet- mality of the residuals. It was determined that all ary treatment were then pooled and homogenized, variables analyzed met the assumptions for para- and subsamples were taken from this composite metric tests, so the same model was used to ana- sample and stored at −20 °C prior to analysis. Diet lyze all the data. The MIXED procedure of SAS samples were analyzed for DM (method 930.15), was used to analyze the data with pen as the experi- CP (method 990.03), ether extract (method 945.16), mental unit and initial BW as a covariate. The fixed and Zn, Ca, P, and Na (method 985.01) at a com- effects were diet, group size, and diet × group size mercial laboratory (Midwest Laboratories, Omaha, interaction. Block was considered a random effect. Nebraska, AOAC, 2007). Bacillus-spore enumer- Differences were considered significant if P < 0.05 ation in diet samples was performed at Midwest and tendencies if 0.05 ≥ P < 0.10. Laboratories using the Bacillus heat shock method (Jackson, 2015). Diets were analyzed for resistant RESULTS starch (RS) content using a commercially avail- able kit (Megazyme, Wicklow, Ireland; method Diet Analysis 2002.02, AOAC 2007). The goal of analyzing diet Results of Zn and RS analysis confirmed their samples for Bacillus, Zn, and RS was to confirm presence in the complete feed in their respective diet- the presence of the additives in the final mixed ary treatments (Tables 1 and 2). With respect to the diets. Diets were not analyzed for the inclusion of DFM product, after the experiment was completed, the acid blend due to the current unavailability of it was discovered that a separate Bacillus-based an assay to quantify the specific acids included in DFM was included in the vitamin–mineral premix the blend. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 304 Olsen et al. used at the commercial feed mill that manufactured compared to large groups fed these diets (P < 0.05). the phase 1 and 2 diets; thus, a DFM product had However, small and large groups had similar ADG been added to all phase 1 and 2 diets. Consequently, for the PC and ZA diets (P > 0.05). The mean ADG Bacillus spore counts were much higher than for large groups was 0.280 kg and was 0.293 kg for expected, although they were also quite variable small groups (main effect P = 0.006). Small groups (data not shown). In the phase 1 and 2 diets, Bacillus had similar ADFI to large groups except for the counts in the DR diet were not as high as expected; NC control diet where small groups had higher recovery varied from 20 to 60% of expected when ADFI (P < 0.05). There was no interaction between taking into account both the DFM in the premix diet and group size for G:F; pigs fed the PC diet and the added DFM in the DR diet. Additionally, were more efficient than pigs fed the NC, ZA, and there was a low recovery of Bacillus in the DR diet DR diets (diet P < 0.001), and small groups were from phase 3, but spore counts were elevated in this more feed efficient than large groups (group size diet compared to the NC, PC, and ZA diets. The P = 0.004). There was no impact of the DR diet on Bacillus product was tested and confirmed to con - growth performance (P > 0.05). tain viable spores very close to the level specified on Within the individual feeding phases, perfor- the product label (91% recovery). All test products mance responses for diet and group size treatments were preweighed and the correct amounts per batch showed similar patterns to the overall treatment were delivered to the feed mills to ensure they were data (data not shown). In phases 1 and 3, no inter- added at the correct quantity. Evaluation of the mix actions between diet and group size were observed sheets confirmed that these preweighed bags were (P > 0.05). The main effect of group size was not indeed added. We cannot explain why the assayed significant for ADG, ADFI, or G:F in phases 1 and spore counts fell short of expected, other than per- 2 (P > 0.10) but was significant in phase 3 where haps the difficulty of assaying low concentrations in small groups had greater ADG and G:F than large complete feed, as compared to a premix. groups (P < 0.01). The main effect of diet was pres- ent in all phases in a similar pattern to the overall results. In phase 3, ADG and G:F were similar to Growth Performance phase 2, which likely reflects depressions in growth Due to naturally occurring health challenges performance due to PRRSV. reported below, overall pig performance was below that expected for this facility (Table 4). Animal Health and Morbidity For the overall period (days 0–41), there were impacts of both dietary treatment and group size, The pigs experienced acute diarrhea and sep- and their interaction, on piglet growth performance. ticemia in the first week of the experiment and a There was an interaction between diet and group PRRSV challenge in the fourth week of the experi- size for ADG (P = 0.012) and ADFI (P =0.015). ment (confirmed by PCR analysis of oral fluids on Pigs fed the PC had higher ADG and ADFI than day 26; Table 3). Mortality was 1.8%, and mor- the NC for both group sizes (P < 0.05), and pigs bidity (pigs removed from the study for illness or fed the ZA diet only had a higher ADG and ADFI injury) was 6.1%. Mortality was not statistically than the NC in the large groups (P < 0.05). Small analyzed due to the low numbers in each treatment. groups fed the NC and DR diets had higher ADG The number of mortalities per treatment was as Table 4. Effects of dietary treatment and group size, and their interaction, on nursery pig growth perfor- mance, day 0–41 Treatment Large group Small group P value Item, kg NC PC ZA DR NC PC ZA DR SEM Diet Group size Diet × group size Start BW 6.12 6.11 6.11 6.12 6.09 6.09 6.09 6.08 0.089 0.997 0.013 0.958 End BW 17.32 20.13 18.25 17.16 18.46 20.01 17.94 17.69 0.361 <0.001 0.154 0.080 ADG 0.26 0.33 0.28 0.25 0.29 0.33 0.27 0.28 0.009 <0.001 0.006 0.012 ADFI 0.40 0.47 0.43 0.40 0.43 0.47 0.42 0.42 0.011 <0.001 0.144 0.015 G:F 0.64 0.69 0.65 0.62 0.67 0.69 0.66 0.66 0.010 <0.001 0.004 0.203 NC = negative control; PC = positive control: NC + dietary antibiotics; ZA = NC + ZnO + dietary acidifier; DR = NC + Bacillus-based direct- fed microbial + 5% resistant starch. Group size treatments: pigs were housed in groups of either 31 (large group) or 11 (small group) pigs per pen. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 Evaluation of antibiotic alternatives 305 follows: NC diet, 8; PC diet, 3; ZA diet, 7; DR diet, so only main effects are presented (Table 6). Pigs 6; large groups: 18; small groups: 6. fed the PC diet required fewer medical treatments On day 5, all pigs were given gentamicin through than pigs fed the NC or DR diet, and the ZA diet the drinking water for 6 d to treat the diarrhea. was intermediate between NC and PC (P = 0.024). Culture of liver and lung tissue from pigs that died There was no effect of group size on number of during this time confirmed exposure to Salmonella medical treatments (P = 0.706). The number of (S. infantitis), Actinobacillus suis, and Streptococcus pigs removed from the study, including mortality suis. Several deaths due to mulberry heart disease and morbidity, was not influenced by dietary treat - prompted water treatment with vitamin E and sele- ment. However, the number of removals was lower nium for 5 d (days 15 to 19). A PRRSV challenge in small groups than in large groups (P = 0.049). was confirmed on day 26 of the study after obser - vations of lethargy, heavy breathing, coughing, DISCUSSION sneezing, and decreased feed intake. Pigs were indi- vidually treated as described in the materials and The swine industry is seeking effective alterna- tives to AGP, and inconsistent results from AGP methods section for symptoms for the remainder of the study. A timeline and result of all necropsies are alternative studies has led to the need for evaluating listed in Table 5; results of all diagnostic testing are AGP alternative testing protocols and study designs. listed in Table 3. The objective of this experiment was to evaluate the There were no interactions between diet and effects of AGP alternative diets and test group size group size for medical treatments or removals, on nursery pig performance. These data can then Table 5. Timeline of necropsies and diagnostic results 1 2 Day Treatment Diagnosis Pathogens confirmed present 3 DR, large group Pneumonia, septicemia Salmonella, Actinobacillus suis, Streptococcus suis 4 ZA, small group Pneumonia, septicemia — 5 ZA, large group Mulberry heart disease — 5 PC, large group Pneumonia, septicemia — 11 ZA, large group Pneumonia, septicemia Mycoplasma hyorhinis 11 DR, large group Pneumonia, meningitis — 13 NC, large group Mulberry heart disease — 17 ZA, large group Pneumonia, septicemia — 17 ZA, large group Mulberry heart disease — 26 NC, large group PRRSV, interstitial pneumonia Streptococcus suis, PRRSV 26 DR, large group PRRSV, interstitial pneumonia Streptococcus suis, PRRSV 38 PC, small group Intestinal torsion — NC = negative control; PC = positive control: NC + dietary antibiotics; ZA = NC+ ZnO + dietary acidifier; DR = NC + Bacillus-based direct- fed microbial + 5% resistant starch. Group size treatments: pigs were housed in groups of either 31 (large group) or 11 pigs per pen (small group). Further testing for specific pathogens at necropsy was done at the discretion of the veterinarian. PRRSV = porcine reproductive and respiratory syndrome virus. Table 6. Effects of dietary treatment and group size on medical treatments and removals, day 0–41 1 2 Diet Group Size Item NC PC ZA DR SEM P value Large Small SEM P value a b ab a Medical treatments, 0.814 0.506 0.719 0.923 0.152 0.024 0.759 0.722 0.136 0.706 3,5 proportion 4,5 Removals, proportion 0.086 0.062 0.073 0.059 0.017 0.666 0.087 0.053 0.0121 0.0486 NC = negative control; PC = positive control: NC + dietary antibiotics; ZA = NC+ ZnO + dietary acidifier; DR = NC + Bacillus-based direct- fed microbial + 5% resistant starch. Group size treatments: pigs were housed in groups of either 31 (large group) or 11 (small group) pigs per pen. Medical treatments calculated as total number of medical treatments administered per pen divided by number of pigs allotted to pen (31 or 11). Removals calculated as total number of pigs removed from study (found dead or removed for illness or injury) divided by number of pigs allot- ted to pen (31 or 11). Means within a row without a common superscript differ significantly ( P < 0.05). Interaction P value for medical treatments and removals not significant. ( P > 0.10). Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 306 Olsen et al. be used to provide a better framework of standards have shown beneficial effects, yet results have been that can be used as a model for future studies testing inconsistent; few studies have looked at these in com- the efficacy of AGP alternatives that will aid in com - bination. Pharmacological levels of Zn have also paring and interpreting results across those studies. proven effective in improving growth performance The majority of published studies evaluating alter- of nursery pigs, in addition to decreasing diarrhea natives to AGP have been conducted in academic (Pettigrew, 2006; Heo et al., 2010; Pérez et al., 2011; research settings, and consequently, most studies Pluske, 2012). Walsh et al. (2007) and Li et al. (2008) have used relatively small groups of pigs (Schweer both reported improvements in growth performance et al., 2017a). The literature review conducted by of nursery pigs due to acidifiers, though Boas et al. Schweer et al. (2017a) showed that experiments with (2016) reported no improvements. Schweer et al. a positive response to an AGP alternative had, on (2017a) reported that acidifiers resulted in ADG average, more pigs per pen than studies that did not improvements in 33.8% of studies. show a positive response. The observed interactions Inclusion of DFM’s has also given inconsistent between diet and group size indicate that consid- responses. Kyriakis et al., (1999), Papatsiros et al. eration of group size may be necessary in studies (2011), and Hu et al., (2014) reported improved evaluating AGP alternatives. Improvements in per- growth performance, but many studies have also formance due to the ZA diet were only detected reported no improvements (Bhandari et al., 2008; when pigs were housed in large groups. Higher Liao and Nyachoti, 2017). Resistant potato starch removal rates were observed when pigs were housed as a prebiotic has been shown to reduce diarrhea in large groups, possibly indicating a higher-stress (Bhandari et al., 2009), and in combination with environment. These results may suggest a greater a DFM has also improved ADG (Krause et al., potential for this combination of additives to be 2010). However, studies evaluating resistant potato effective under higher-stress situations, which may starch are uncommon. occur in larger group sizes. Furthermore, the bene- It is clear that the PRRSV challenge impacted fit of AGP seemed smaller when pigs were housed the performance of this group of pigs. Based on the in small groups. Small groups fed the NC and DR standard feed budget used at this farm, expected diets had increased ADG compared to large groups. feed intake during phase 3 would be 1.0–1.2 kg/ The PC and ZA diets seemed to somewhat com- pig/day. Pigs consumed, on average, only 0.52 kg/ pensate for slower gain in large groups as small pig/day during this period. Compared to estimates and large groups had similar ADG when fed these from NRC (2012) for 11–25 kg pigs, the pigs gained diets. Improved growth performance when pigs are 46% less and ate 45% less per day. However, in housed in smaller groups is in agreement with pre- phases 1 and 2, prior to the PRRSV outbreak, pigs vious reports of this trend in nursery pigs (Wolter performed as expected (0.212 kg/day compared et al., 2000, 2001). McGlone and Newby (1994) also to the 0.21 kg/day estimate for 5–7 kg pigs, and reported higher morbidity rates in pens of 40 pigs 0.31 kg/day compared to the 0.34 kg/day estimate compared to pens of 10 or 20. These results indicate for 7–11 kg pigs; NRC, 2012). Severely reduced that group size may impact the outcomes of AGP feed intake and low growth rate demonstrates the alternative studies, and perhaps positive responses impact of the PRRSV challenge on growth perfor- to specific AGP alternatives are less pronounced in mance, which is typical for pigs challenged with this studies where pigs are housed in smaller groups. virus (Schweer et al., 2017b). The present results The growth-promoting effects of subtherapeu- were likely influenced by this health challenge, espe - tic levels of antibiotics in swine diets are well docu- cially in phase 3 when pigs were consuming far less mented (Cromwell, 2002). Improvements in ADG, feed than expected and therefore were not receiving ADFI, and G:F observed in this study due to AGP the desired amount of the AGP alternatives, poten- inclusion are similar in magnitude to previous reports tially decreasing their effect. (Cromwell, 2002). The current improvements are Pigs fed the PC diet required almost 40% fewer higher than the values reported by Dritz et al. (2002) medical treatments, suggesting that AGP were which could be due to the poor performance of the beneficial to pig health and welfare during a dis - NC treatment, perhaps due to health status. It should ease challenge. The number of medical treatments also be noted that the chlortetracycline inclusion required when pigs were fed the ZA diet was inter- level in the present diets is higher than some previous mediate between the NC and PC diets, indicating studies have used, but the levels of antibiotics used that this diet may have also benefited pig health. in this study were compliant with the 2017 VFD for Few studies report medical treatments, but Pérez this particular farm. Separately, ZnO and acidifiers et al. (2011), as an example, reported a decrease in Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 Evaluation of antibiotic alternatives 307 the number of required medical treatments for pigs response to AGP alternatives (Allen et al., 2013; Boas fed ZnO during a pathogenic E. coli challenge. et al., 2016). Some studies have shown the potential for AGP alternatives to mitigate a health challenge (Bhandari et al., 2008; Gebru et al., 2010; Heo et al., Considerations for Future Studies 2010); benefits of AGP alternatives to animal health There are likely many factors responsible for the during a disease challenge would be of great interest inconsistent responses observed in studies evaluat- to the swine industry. Thus far, the impact of specific ing AGP alternatives (Allen et al., 2013; Thacker, AGP alternatives in the presence of particular path- 2013). To increase the value of future studies, it ogens is not well understood, and information about will be highly beneficial to provide more informa - health status is mostly absent in published AGP alter- tion on study conditions than has previously been native studies (Schweer et al., 2017a). Documentation the case. When such information is provided, the of the pathogens present in a group of pigs that may context of the study will be more apparent, and it influence the outcome of a study will help to build will be much easier to compare studies conducted an understanding of how AGP alternatives may per- in different locations and in different environments. form under varying health conditions. In this study, Figure 3 outlines proposed necessary components the collection of oral fluid and serum samples as well that should be included and reported in AGP alter- as necropsies of pigs that died allowed for the iden- native studies. The remainder of this discussion will tification or exclusion of critical pathogens, includ - elaborate on a few specific components. ing PRRSV, as influential factors in this group of Health status is an important consideration pigs. Collection and testing of diagnostic samples, when alternatives are being evaluated, as prod- especially at the beginning and end of a study, can ucts may have greater or less efficacy under certain be used to assess and document pathogen exposure. health conditions. Some evidence exists to suggest If clinical signs of illness are observed, additional that AGP are more effective on commercial farms samples should be collected, based on the symptoms, than in academic-type research settings (Cromwell, to characterize the illness. Major changes in health 2002; Dritz et al., 2002), and this has been hypothe- status throughout a trial should be reported. Table 7 sized to be partially due to lower pathogen load and outlines examples of potential pathogens of interest incidences of “subclinical” disease (Zimmerman, and methods of testing for them. 1986). If health status can affect the response to Determining pathogen presence, or the presence AGP, then it is logical to propose that it could also of agents/active infections, will involve identifying influence the effects of AGP alternatives as well. genetic material of a pathogen (generally through Indeed, health status has been discussed repeat- PCR), detecting an antigen (through ELISA or immu- edly as a potential reason for inconsistencies in nohistochemistry), or detecting a viable pathogen Figure 3. Proposed necessary study components to be included and reported in studies evaluating alternatives to antibiotic growth promoters (AGP) for pigs. When critical information is included in reports of AGP alternative studies, the context of the study is better understood. This will aid in making comparisons across multiple studies and will lead to faster and more valuable conclusions about the effectiveness of AGP alternative products. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 308 Olsen et al. Table 7. Examples of methods for determining Table 8. Sample size calculations pathogen exposure in studies Variable Group size SD Effect size Sample size (n/trt) 1 2 ADG, kg 31 Pigs/pen 0.036 0.05 9 Pathogen Sample to test Testing method 11 Pigs/pen 0.032 0.05 7 PRRSV Oral fluids, or serum PCR, abELISA (or both) ADFI, kg 31 Pigs/pen 0.042 0.07 6 PEDV Oral fluids PCR 11 Pigs/pen 0.032 0.07 4 Serum abELISA G:F 31 Pigs/pen 0.036 0.05 9 PDCoV Oral fluids PCR 11 Pigs/pen 0.038 0.05 10 IAV Oral fluids PCR α = 0.05; power = 0.80. Serum abELISA Estimates of SD associated with each group size (31 or 11 pigs/pen) Mycoplasma Deep swab PCR obtained from current experiment (days 0–41 data was used). hyopneumoniae Oral fluids PCR Serum abELISA diets. Thus, the phase 1 and 2 diets all had greater Porcine circovirus Oral fluids PCR spore counts than expected. Additionally, the spore Serum abELISA, PCR counts in all the phase 1 and 2 diets were unexpect- Mycoplasma hyorhinis Oral fluids PCR edly variable, and overall recovery was low (ranging Haemophilus parasuis Oral fluids PCR Rotavirus Oral fluids PCR from 20% to 50% in phase 1 and 2 diets; DR diets TGEV/ PRCV Oral fluids PCR had an average recovery of 23% in phases 1 and Lawsonia intracellularis Oral fluids, feces PCR 2). This made it difficult to determine if the DFM Actinobacillus Serum Serology product was correctly added to the DR diets. It was pleuropneumoniae Tonsil scrape PCR clearer that the DFM product was added correctly Salmonella Serum, feces, rectal Serology culture, in the phase 3 diets, although recovery of the prod- swab PCR uct was not as high as expected (roughly 30%) and E. coli Rectal swab Culture may also point to variability or low recovery of the Brachyspira Rectal swab Culture, PCR Bacillus assay in general. Actinobacillus suis Nasal swab Culture, PCR To the authors’ knowledge, there is currently Streptococcus suis Lung Culture no assay readily available to analyze for the specific PRRSV = porcine reproductive and respiratory syndrome virus, acids contained in the acid blend that was used in PEDV = porcine epidemic diarrhea virus, PDCoV = porcine deltacor- this experiment. Zinc levels in the ZA diets were onovirus, IAV = influenza A virus, TGEV/PRCV = transmissible gas - troenteritis virus/porcine respiratory coronavirus. slightly lower than expected but were much higher in PCR = polymerase chain reaction, abELISA = ELISA for antibody the ZA as intended (Table 1). When considering the detection. RS content of the potato starch product (approxi- mately 78%, DM basis), the DR diet in phases 1 through isolation (Christopher-Hennings et al., 2012). and 2 showed only 62% recovery of expected values Pathogen exposure is determined by measuring sero- of RS. Since these were pelleted, the low recovery conversion, which confirms a prior infection or pres - could be due to heat and water application dur- ence of a maternal antibody and is done by detecting ing the pelleting process, which can cause starch antibody in the serum (Christopher-Hennings et al., to gelatinize and increase its susceptibility to deg- 2012). The specific procedure for defining health radation by alpha-amylase (Svihus and Zimonja, status via pathogen presence or exposure will likely 2011). When possible, it is crucial to analyze diets depend on the nature of a study and the pathogens for the AGP alternatives being tested to confirm involved, and a strategy may need to be adapted for their presence as intended, as these outcomes can each study and pathogen of interest. It is also impor- influence the interpretation of study results. tant to report the medical treatment regimen used if With future study design in mind, sample size pigs need to be treated for illness. calculations were conducted (Table 8) using the SD While it is important to confirm the presence generated in the overall data to predict the sample of feed additives through diet analysis, it may not size that would be needed to detect differences of be possible to be fully quantitative in this respect, practical significance and to determine if required due perhaps to limitations of the assay, or due to sample size would differ according to pig group transformation of the additive during the feed size. Though group size may be an important con- manufacturing process. In this study, analysis of sideration in AGP alternative studies as previously feed samples for Bacillus spore counts revealed that discussed, it does not appear that a larger sample a Bacillus product was included in the vitamin– size would necessarily be needed for one pig group mineral premix that was used in the phase 1 and 2 size over the other. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018 Evaluation of antibiotic alternatives 309 doi:10.2460/javma.2002.220.1690 In conclusion, the methodology used in this Gebru, E., J. S. Lee, J. C. Son, S. Y. Yang, S. A. Shin, B. study resulted in the ability to compare the impact Kim, M. K. Kim, and S. C. Park. 2010. 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Sci. 62 (Suppl. 3):6– (Suppl. 1):147–148. doi:10.2527/asasmw.2017.303 16. doi:1986.62supplement_36s Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/298/5049815 by Ed 'DeepDyve' Gillespie user on 31 July 2018
Translational Animal Science – Oxford University Press
Published: Sep 1, 2018
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