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Effects of water and diet acidification with and without antibiotics on weanling pig growth and microbial shedding^1,2

M. C. Walsh^*, D. M. Sholly^*, R. B. Hinson^*, K. L. Saddoris^*, A. L. Sutton^*, J. S. Radcliffe^*, R. Odgaard^,3, J. Murphy and B. T. Richert^*,4

^* Department of Animal Science, Purdue University, West Lafayette, IN 47907; and and Kemin AgriFoods North America, Des Moines, IA 50317

	Abstract

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Two 5-wk experiments were conducted to determine the effects of water and diet acidification with and without antibiotics on weanling pig growth performance and microbial shedding. In Exp. 1, 204 pigs (19.2 d of age) were used in a 3 x 2 factorial, with 3 dietary treatments fed with or without water acidification (2.58 mL/L of a propionic acid blend; KEM SAN, Kemin Americas, Des Moines, IA). Dietary treatments were: 1) control, 2) control + 55 ppm of carbadox (CB), and 3) dietary acid [DA; control + 0.4% organic acid-based blend (fumaric, lactate, citric, propionic, and benzoic acids; Kemin Americas)] on d 0 to 7 followed by 0.2% inorganic acid-based blend (phosphoric, fumaric, lactic, and citric acids; Kemin Americas) on d 7 to 34. In Exp. 2, 210 pigs (average 18.3 d of age) were fed 1 of 3 dietary treatments: 1) control, 2) control + 55 ppm of CB, and 3) control + 38.6 ppm of tiamulin + 441 ppm of chlortetracycline on d 0 to 7 followed by 110 ppm of chlortetracycline on d 7 to 35 (TC) with or without dietary acidification (same as Exp. 1) in a 3 x 2 factorial arrangement of treatments. For both experiments, the pigs were allotted based on genetics, sex, and initial BW [5.5 kg (Exp. 1) or 5.6 kg (Exp. 2)]. Pigs were housed at 6 or 7 (Exp. 1) and 7 (Exp. 2) pigs/pen. Treatments were fed in 3 phases: d 0 to 7, 7 to 21, and 21 to 35 (34 d, Exp. 1). Fecal grab samples were collected from 3 pigs/pen on d 6, 20, and 33 for measurement of pH and Escherichia coli. During phase 3 and overall in Exp. 1, pigs fed CB had greater (P < 0.001) ADG (overall ADG, 389 vs. 348, and 348 g/d, respectively), ADFI (P < 0.007, 608 vs. 559, and 554 g/d, respectively), and d 34 BW (P < 0.001, 18.8 vs. 17.3, and 17.3 kg, respectively) than pigs fed NC and DA. Phase 3 ADG was improved (P < 0.01) by water acidification across all diets. In Exp. 2, pigs fed CB and TC had greater ADG (P < 0.004; 315 and 303 vs. 270 g/d, respectively), ADFI (P < 0.01), and d 35 BW (P < 0.002; 16.7 and 16.2 vs. 15.1 kg, respectively) than pigs fed NC. There was a tendency (P < 0.08) for an improvement in ADG when DA was added to the NC or TC, but decreased ADG when DA was added to CB.

Key Words: acid • carbadox • Escherichia coli • tiamulin • weanling pig

	INTRODUCTION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
One of the main issues affecting profitability of the swine industry is loss in production efficiency resulting from the lag in growth at weaning. Intensification of swine production has resulted in a reduction in the suckling period from 4 to 5 wk to 2 to 3 wk in an attempt to maximize annual sow productivity. Young pigs are susceptible to gastrointestinal disorders and digestive disturbances as a result of their immature digestive system. A side effect of this is an increase in the prevalence of postweaning scours, which leads to retarded growth, increased mortality, and additional medical costs (Aumaître et al., 1995; Cranwell, 1995; Jahn and Uecker, 1997).

This problem has been combated through the use of subtherapeutic doses of antibiotics in feed, which have been shown to improve the growth rate of weanling pigs (Hays, 1978; Zimmerman, 1986; Cromwell, 1991). However, increasing public concern in relation to food safety issues and antibiotic resistance has prompted the swine industry to look for alternatives to the use of antibiotics in nursery pig diets. Diet acidifiers have been reported to reduce digestive scouring (White et al., 1969) and the concentration of coliform populations along the gastrointestinal tract (Cole et al., 1968; Thomlinson and Lawrence, 1981).

The objectives of the present studies were to evaluate the efficacy of organic and inorganic acid-based blends as alternatives to antibiotics as dietary and water acidifiers. An additional objective was to assess the possible additive effects of acidifiers and antibiotics on weanling pig growth performance and microbial shedding.

	MATERIALS AND METHODS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
All animals were cared for in accordance with Purdue University Animal Care and Use Committee regulations.

A total of 414 pigs (Exp. 1, n = 204; Exp. 2, n = 210) weaned at an average of 19.2 (Exp. 1) and 18.3 (Exp. 2) d of age were used in two 5-wk experiments to evaluate the effects of water and diet acidification with or without antibiotics on weanling pig growth performance and microbial shedding. Experimental procedures for both experiments were similar, with the exception of the dietary treatments. Pigs were housed at 6 or 7 (Exp. 1) and 7 (Exp. 2) pigs/pen.

Dietary Treatments
In Exp. 1, pigs were assigned to 3 dietary treatments: 1) control, 2) control + 55 ppm of carbadox, and 3) control + dietary acids (control + 0.4% organic acid-based blend for d 0 to 7 followed by 0.2% inorganic acid-based blend for d 7 to 34; Kemin AgriFoods North America, Des Moines, IA). These 3 dietary treatments were factored with or without water acidification of an organic acid-based blend [2.58 mL/L of drinking water; KEM SAN (predominantly propionic, acetic, and benzoic acids), Kemin Americas] in a 3 x 2 factorial arrangement. In Exp. 2, 3 dietary treatments were fed: 1) control; 2) control + 55 ppm of carbadox, and 3) control + 38.6 ppm of tiamulin and 441 ppm of chlortetracycline (CTC) for d 0 to 7, followed by 110 ppm of CTC from d 7 to 35. These 3 treatments were factored with or without dietary acids (as in Exp. 1) for d 0 to 35, in a 3 x 2 factorial arrangement.

Animal and Feeding Management
The pigs were allotted based on genetics, sex, and initial BW [average = 5.5 kg (Exp. 1) and 5.6 kg (Exp. 2)]. All pigs had unlimited access to feed and water through a 5-hole self-feeder and a single nipple waterer in each pen. Phase 1, 2, and 3 diets were fed from d 0 to 7, d 7 to 21, and d 21 to 34 (Exp. 1) or 35 (Exp. 2), respectively (Tables 1 and 2). All diets were formulated to meet or exceed the estimated nutrient requirements for pigs (NRC, 1998). Experimental treatments were continued during all 3 phases. For calculation of ADG, ADFI, and G:F, the pigs were individually weighed, and feed disappearance was recorded weekly for each pen.

The procedure used for enumeration of E. coli was as follows. A 1-g subsample of each pen composite, fecal sample was mixed into 9 mL of peptone broth, serially diluted, and used to inoculate MacConkey agar plates for E. coli isolation. The E. coli plates were inoculated at 3 dilutions and in triplicate using the spread plating technique. Before plating, the samples were serially diluted to 10⁵, 10⁶, and 10⁷ cfu/mL for samples collected on d 6; 10⁴, 10⁵, and 10⁶ cfu/mL for samples collected on d 20; and 10³, 10⁴, and 10⁵ cfu/mL for samples collected on d 33. The MacConkey agar plates were incubated for 24 h at 37°C, and after removal from the incubator, the E. coli colonies were immediately counted.

In Exp. 1, 2 pooled water samples per treatment were collected on d 5 and 32 and analyzed for pH, iron content, total coliforms, and water acid concentration by Kemin Americas Inc. In addition, pig water usage was monitored by a water meter at the source of each water treatment.

Statistical Analysis
Data sets for each experiment were analyzed as a completely randomized block design, with a 3 (dietary treatments) x 2 (levels of supplemental acidification) factorial arrangement using the GLM procedure (SAS Inst. Inc., Cary, NC). For all response criteria, pen was the experimental unit. Dietary treatment effect was tested against the residual error term with initial BW used as a blocking factor. Main effects are described, except when interactions were detected. Simple means are presented when interactions were observed. To enhance interpretation of results, means separation was conducted when the dietary treatment main effect reached a significance level of P < 0.10, using the Duncan’s multiple range test with P < 0.05 and P < 0.10 levels of significance.

	RESULTS

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Experiment 1
Water Analysis.
The water acidification treatment was added near the target rate of 2.58 mL/L based on analysis of water samples averaging 2.50 mL/L (Table 3). Water acidification decreased water pH by 36.5% and increased iron content of the water. Acidified and nonacidified water contained extremely low levels of coliforms with less than 10 cfu/mL of total coliforms. Water acidification increased water usage by 47% (5.83 vs. 3.96 L·pig^–1·d^–1) compared with the control water treatment.

During phase 3 (d 21 to 34), pigs fed carbadox had greater (P < 0.001) ADG and ADFI than pigs fed dietary acid or the control diet (ADG: 600 vs. 552, and 539 g/ d, respectively). Feed efficiency of pigs fed dietary acid during phase 3 tended (P < 0.09) to be greater than pigs fed the control diet but was not different from pigs fed carbadox. At the end of phase 3 (d 34), pigs fed carbadox were heavier (P < 0.001) than pigs fed dietary acids or the control diet (18.8 vs. 17.4, and 17.4 kg, respectively). During phase 3, pigs receiving water acidification had greater (P < 0.01) ADG (576 vs. 551 g/d; Table 5) and ADFI than pigs receiving no water acidification. Additionally, there was an interaction between dietary treatments and water acidification for phase 3 ADFI (P < 0.04). The ADFI was similar when dietary acid was fed with or without acidified water, whereas pigs fed carbadox and the control responded to water acidification by increasing ADFI.

Overall (d 0 to 34) there was a main effect of diet whereby pigs fed carbadox had greater (P < 0.001) ADG than pigs fed dietary acid or the control (389 vs. 348, and 348 g/d, respectively). Throughout the experiment, pigs fed carbadox also had greater (P < 0.007) ADFI than pigs fed dietary acid or the control (608 vs. 554, and 559 g/d, respectively). Overall, there was no effect of diet on G:F. Pigs receiving no water acidification had greater G:F (P = 0.03) than pigs receiving water acidification (Table 5). There was a tendency for an interaction between diet and water acidification for ADFI (P < 0.08). Overall, when pigs were fed carbadox and the control, water acidification increased ADFI. However, when pigs were fed dietary acid, water acidification decreased ADFI.

Fecal E. coli Concentrations and pH.
There were no effects of diet or water treatments on fecal E. coli shedding on d 6, 20, or 33 of the experiment (Table 6 and 7). Dietary treatment had no effect on fecal pH at d 6, 20, or 33. Similarly, there was no effect of water acidification on fecal pH at d 6 and 20. However, on d 33, pigs receiving water acidification tended (P < 0.10) to have lower fecal pH than pigs consuming nonacidified water (6.08 vs. 6.21). No diet x water acidification interactions for E. coli shedding or fecal pH were observed.

Overall (d 0 to d 35), pigs fed an antibiotic in their diet, carbadox or tiamulin + CTC, had greater ADG (P < 0.004) than control pigs (315 and 303 vs. 270 g/d, respectively). Throughout the trial, control pigs had lower (P < 0.012) ADFI than pigs fed carbadox or tiamulin + CTC (459 vs. 520, and 508 g/d, respectively). Overall, pigs receiving no dietary acidification tended (P < 0.06) to have greater G:F than pigs fed acidified diets (Table 9). However, there were no main effects of diet acidification on ADG and ADFI. There was a tendency for an interaction between dietary treatment and acidification for overall ADG (P < 0.08). When pigs were fed the control diet or tiamulin + CTC, dietary acidification increased ADG compared with no dietary acidification. However, when pigs were fed carbadox, dietary acidification decreased ADG compared with no dietary acidification.

Fecal E. coli Concentration and pH.
There were no effects of dietary treatment or dietary acidification on E. coli shedding on d 6 or 20 (Table 10 and 11). Pigs fed carbadox shed lower concentrations of E. coli on d 33 (P < 0.001) compared with control pigs or pigs fed tiamulin + CTC. Pigs receiving no dietary acidification tended to have lower E. coli concentrations (P = 0.09) compared with pigs fed acidified diets on d 33. There was no effect of dietary treatment or dietary acidification on fecal pH on d 20 or 33. Pigs fed tiamulin + CTC had lower fecal pH (P < 0.002) than control pigs or pigs fed carbadox on d 6. Fecal pH on d 6 also tended (P < 0.07) to be lower in pigs receiving no dietary acidification compared with pigs fed acidified diets (6.65 vs. 6.85). There were no dietary treatment by dietary acidification interactions on E. coli shedding or fecal pH.

	DISCUSSION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

In Exp. 1 and 2, carbadox diets tended to reduce E. coli shedding on d 33 compared with pigs fed all other dietary treatments. Although antibiotics have proven successful in reducing ammonia in the circulatory system, disease control is the most commonly accepted mode of action, which concurs with results from the current studies. Hays and Speer (1960) observed that antibiotics were more effective at disease control under poor environmental conditions with high disease pressure compared with more sanitary, well-managed conditions.

Tiamulin and CTC are commonly used in an antibiotic program for growth promotion in weanling pigs, which involves the combination of tiamulin (38.6 ppm) and CTC (441 ppm) for d 0 to 14 postweaning followed by CTC (110 ppm) alone for the remainder of the nursery period. Keegan et al. (2003) observed that nursery pigs fed tiamulin and CTC in feed had greater gains and feed intake than pigs fed carbadox, neo-terramycin, or a nonmedicated diet during a 31-d trial. Burch et al. (1986) reported greater ADG for pigs fed tiamulin and CTC than for pigs fed CTC alone. Results from Exp. 2 agree with these findings, reporting increases in both ADG and ADFI when pigs were fed tiamulin and CTC compared with control-fed pigs.

In addition to influencing growth performance, antibiotics have been reported to reduce microbial loads in the gastrointestinal tract (Owusu-Asiedu et al., 2003). Bacteria produce amines, which have been reported to be a causative agent for postweaning diarrhea in pigs (Porter and Kenworthy, 1969). Ammonia resulting from microbial amino acid degradation and urea hydrolysis may interfere with epithelial cell turnover (Visek, 1972, 1978a) and depress growth performance of pigs (Visek, 1978b). Consequently, in the absence of a large microbial load and associated ammonia and amine production, maturation of the pig digestive system and its ability to secrete HCl develops more readily (Kidder and Manners, 1978). In Exp. 2, pigs fed tiamulin and CTC and carbadox tended to have lower fecal pH on d 6 compared with pigs receiving nonmedicated feed, which may be explained in part by the findings of Kidder and Manners (1978).

Organic or inorganic acids, or both, can be delivered to weanling pigs through the feed or water. Cole et al. (1968) reported improvements in ADG and feed efficiency of weanling pigs with addition of lactic acid (0.8%) in the drinking water. Additionally, Daniels (1983) observed that drinking water acidified with propionic acid resulted in a 2-kg heavier pig at the end of the nursery phase. In Exp. 1, the addition of 2.58 mL/ L of an organic acid-based blend to pigs in drinking water increased ADG across all treatment groups during phase 3 (d 21 to 34). This suggests that the effectiveness of water acidification improves as the pig matures or as the diet complexity is reduced. In this study, water acidification increased pig feed intake when carbadox and nonmedicated diets were fed; however, the inclusion of dietary acidifiers negated the effects of water acidification. Depressed feed intakes observed when diet and water acidification were combined may be the result of decreased palatability arising from high levels of acid. Radecki et al. (1988) reported that high levels of citric acid had a negative effect on feed intake. Previous research from our laboratory (Walsh et al., 2004) also provides evidence to support this claim whereby feed intake was reduced when dietary acidifiers (organic and inorganic acid-based blends) were included at 0.6% in weanling pig diets.

In Exp. 1, pigs receiving no water acidification had greater G:F than pigs receiving acidified drinking water. Water acidification increased water usage by 47%; however, no statistics were carried out, so the increase in water usage cannot be definitely linked to a decrease in G:F. Overall in Exp. 1, there tended to be a carbadox x water acidification interaction for feed intake. Pigs fed carbadox responded to water acidification by increasing their feed intake. Coincidently, the addition of a dietary acidifier to pigs fed a diet containing carbadox in Exp. 2 resulted in a reduction in overall ADG compared with pigs fed carbadox alone. These results suggest that carbadox-fed pigs maybe sensitive to the route of acidifier administration.

Acidification of weanling pig diets with organic and inorganic acids, particularly fumaric and citric acids, lowers diet pH and has resulted in improved growth performance. Dietary acid blends may be more beneficial than individual acids alone as a result of a broader spectrum of activity. In 2003, Namkung et al. reported similar growth performance to medicated treatment groups when organic acid-based blends were fed to weanling pigs. An earlier study conducted using a phosphoric acid-based acidifier containing other organic acids in a blend (citric, lactic and fumaric acid) increased growth performance of weanling pigs but was not different from fumaric acid alone (Schoenherr, 1994). However, the performance of pigs fed acidified diets in Exp. 1 was not different from negative control-fed pigs. Similar results were reported by Radecki et al. (1988) who observed no beneficial effects of citric acid on growth performance and feed intake was reduced. Likewise, Falkowski and Aherne (1984) observed a 4 to 7% improvement in growth rate as a result of 1 or 2% fumaric acid inclusion; however, this increase was not significant. It is possible that the variability in results is a consequence of other factors such as disease pressure, environmental stress, etc., influencing the effectiveness of dietary acids. In Exp. 2 a tendency for a dietary acidification by dietary treatment interaction was observed. Overall, the addition of dietary acidifiers improved ADG in pigs fed the negative control diet and the tiamulin + CTC; however, no improvement in ADG was observed with the carbadox diet. Tiamulin and CTC function primarily against respiratory pathogens such as bacterial pneumonia, etc., commonly found in modern pig production systems (Burch et al., 1986). Conversely, carbadox has been shown to be more effective at reducing the incidences of postweaning diarrhea caused by E. coli (Holmgren, 1994). It is possible that dietary acidifiers can function synergistically with tiamulin and CTC and not with carbadox because they function differently. Both carbadox and diet acidifiers carry out their function via alterations in gut microflora and the encouragement of nutrient sparing; therefore, no additive effects were observed. In contrast, tiamulin and CTC address respiratory disease challenges and dietary acidifiers address bacterial challenge in the gastrointestinal tract. Therefore, by targeting 2 routes of infection, diet acidifiers and tiamulin and CTC may have an additive effect.

Numerous studies have reported that adding organic acids to the diets may reduce coliform burden along the gastrointestinal tract (Thomlinson and Lawrence, 1981; Mathew et al., 1991) and thereby reduce scouring and piglet mortality. In agreement with these findings, pigs fed acidified diets in Exp. 2 were had lower fecal pH on d 6 and E. coli shedding on d 33 compared with pigs receiving no dietary acidification.

Addition of dietary acidifiers in conjunction with some antibiotics may have beneficial effects on ADG. Addition of dietary acidifiers to a diet containing tiamulin and CTC resulted in an 83% recovery of the carbadox response compared with only 40% when tiamulin and CTC were fed alone. Dietary acidifiers alone were able to recover 12% of the carbadox ADG response. These results demonstrate the potential for the individual use of dietary and water acidification to improve nursery pig growth performance in antibiotic-free diets and may further improve pig performance when pigs are being fed an antibiotic. However, no changes in E. coli shedding or fecal pH were observed.

	Footnotes

 
¹ ARP #2006-17983.

² Financial support provided in part by Kemin AgriFoods North America, Des Moines, IA.

³ Current address: Pharmtech International, Des Moines, IA.

⁴ Corresponding author: brichert{at}purdue.edu

Received for publication January 26, 2006. Accepted for publication January 21, 2007.

	LITERATURE CITED

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 


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