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. 2023 May 23;7(1):txad055. doi: 10.1093/tas/txad055

Effect of added calcium carbonate without and with benzoic acid on weanling pig growth performance, fecal dry matter, and blood Ca and P concentrations

Alan J Warner 1, Joel M DeRouchey 2, Mike D Tokach 3, Jason C Woodworth 4, Robert D Goodband 5,✉, Jordan T Gebhardt 6
PMCID: PMC10319757  PMID: 37415595

Abstract

The objective of these studies was to determine the effects of increasing levels of calcium carbonate (CaCO3) with and without benzoic acid on weanling pig growth performance, fecal dry matter (DM), and blood Ca and P concentrations. In experiment 1, 695 pigs (DNA Line 200 × 400, initially 5.9 ± 0.02 kg) were used in a 28 d study. Pigs were weaned at approximately 21 d of age and randomly assigned to pens and then pens were allotted to one of five dietary treatments. Treatment diets were fed from weaning (day 0) to day 14, with a common diet fed from days 14 to 28. Dietary treatments were formulated to provide 0%, 0.45%, 0.90%, 1.35%, and 1.80% added CaCO3 at the expense of ground corn. From days 0 to 14 (treatment period), average daily gain (ADG) and G:F decreased (linear, P ≤ 0.01) as CaCO3 increased. From days 14 to 28 (common period) and for the overall experiment (days 0 to 28), there was no evidence of differences in growth performance between treatments. For fecal DM, there was a trend (quadratic, P = 0.091) where pigs fed with the highest CaCO3 diets had the greatest fecal DM. Experiment 2 used 360 pigs (DNA Line 200 × 400, initially 6.2 ± 0.03 kg) in a 38 d study. Upon arrival to the nursery facility, pigs were randomly assigned to pens and then pens were allotted to one of six dietary treatments. Dietary treatments were fed in three phases with treatment diets fed from days 0 to 10 and days 10 to 24, and a common phase 3 diet fed from days 24 to 38. Dietary treatments were formulated to provide 0.45%, 0.90%, and 1.35% added CaCO3 with or without 0.5% benzoic acid (VevoVitall, DSM Nutritional Products, Parsippany, NJ) added at the expense of ground corn. There was no evidence (P > 0.05) for any CaCO3 by benzoic acid interactions. For the experimental period (days 0 to 24), there was a tendency for benzoic acid to increase ADG (P = 0.056), average daily feed intake (ADFI; P = 0.071), and gain-to-feed ratio (G:F; linear, P = 0.014) as CaCO3 decreased. During the common period (days 24 to 38), pigs previously fed benzoic acid had increased (P = 0.045) ADG and marginally increased (P = 0.091) ADFI. For the overall study, pigs fed benzoic acid had increased ADG (P = 0.011) and ADFI (P = 0.030), marginally increased G:F (P = 0.096) and final body weight (P = 0.059). Serum Ca decreased (linear, P < 0.001) as CaCO3 decreased in the diet. These data show that decreasing the CaCO3 content in the nursery diet immediately after weaning may improve ADG and G:F. Dietary addition of benzoic acid may also provide beneficial effects on ADG and ADFI, regardless of dietary Ca level.

Keywords: acid binding capacity, benzoic acid, calcium, calcium carbonate, growth, nursery pig

Lowering the calcium carbonate levels in weanling pig diets improved daily gain and gain-to-feed. Also, dietary addition of benzoic acid increased average daily gain and feed intake.

INTRODUCTION

Acid binding capacity (ABC-4) is a feed ingredient’s ability to resist a change in gastrointestinal tract (GIT) pH. A high ABC-4 is associated with high pH when the ingredient is suspended within an aqueous solution. A high gastric pH has been observed to result in GIT challenges including increased intestinal bacteria such as Escherichia coli (Smith and Jones, 1963) whereas a low stomach pH improves protein digestion (Kil et al., 2011) and intestinal health (Li et al., 2008).

Although Ca is important to maximize bone mineralization (Lagos et al., 2019) and other physiological functions (Crenshaw, 2001), certain Ca containing ingredients have a high ABC-4. Calcium carbonate (CaCO3) is one such ingredient with a relatively high ABC-4 (Jasaitis et al., 1987; Lawlor et al., 2005). Calcium carbonate has an ABC-4 of 12,932 mEq/kg, whereas other ingredients such as corn, soybean meal, corn DDGS, and dicalcium phosphate have lower ABC-4 (111, 642, 96, and 3,098 mEq/kg, respectively; Lawlor et al., 2005). An improvement in growth performance has been observed with lower dietary ABC-4 (Lawlor et al., 2006).

To help lower gastric pH, dietary acidifiers have been extensively evaluated. Benzoic acid has been observed to decrease E. coli in the lower GIT (Guggenbuhl et al., 2007; Diao et al., 2021) and improve growth performance (Guggenbuhl et al., 2007; Chen et al., 2017; Bergstrom et al., 2020; Bradley et al., 2020). Benzoic acid has also been observed to lower the pH of the stomach and lower GIT organs of nursery pigs (Kluge et al., 2006; Halas et al., 2010). Our hypothesis was that short-term reduction in dietary CaCO3, and the addition of benzoic acid would decrease dietary ABC-4 resulting in increased pig performance. Therefore, the objective of this study was to investigate the effects of increasing levels of CaCO3 and the interactive effects of CaCO3 level with or without benzoic acid on the growth performance, fecal dry matter (DM), and blood Ca and P concentrations of nursery pigs.

MATERIALS AND METHODS

The Kansas State University Institutional Animal Care and Use Committee approved the protocols (4035) used in these experiments. The studies were conducted at the Kansas State University Segregated Early Weaning Facility in Manhattan, KS. The facility has two identical barns that are completely enclosed, environmentally controlled, and mechanically ventilated. Each pen contained a four-hole, dry self-feeder, and a cup waterer to provide ad libitum access to feed and water. Pens (1.22 × 1.22 m) had metal tri-bar floors and allowed approximately 0.30 m2/pig.

Animals and Diets

Experiment 1.

A total of 695 castrated male pigs (DNA Line 200 × 400, Columbus, NE; initially 5.9 ± 0.02 kg) were used in two groups in a 28-d study with 5 pigs per pen and 27 or 28 replications (pens) per treatment. There were 350 and 345 pigs in group 1 and 2, respectively. Upon arrival to the nursery research facility, pigs were randomly assigned to pens and then pens were allotted to one of five dietary treatments. Treatment diets were fed from days 0 to 14 and a common phase 2 diet was fed from days 14 to 28. Dietary treatments were formulated to provide 0%, 0.45%, 0.90%, 1.35%, or 1.80% added CaCO3 at the expense of ground corn (Table 1). The calculated dietary Ca levels were 0.49%, 0.66%, 0.84%, 1.01%, and 1.18%, which were below and above the total Ca requirement estimate of 0.85 and 0.80 for 5 to 7 and 7 to 11 kg pigs (NRC, 2012). Standardized total tract P concentration was maintained well above NRC (2012) requirement estimates to account for the high Ca levels decreasing P absorption (Wu et al., 2018). The corresponding dietary ABC-4 values of 424, 481, 539, 597, and 655 mEq/kg, respectively. Treatment diets were fed in meal form for group 1 and pellet form for group 2, with the common phase 2 diet fed in meal form in both groups. At the time of manufacturing for each group, a single base diet was manufactured at Hubbard Feeds in Beloit, KS, packaged in 22.7 kg bags and then transported to Manhattan, KS, where CaCO3 and corn additions were mixed with the base diet to form experimental treatments. In group 2, diets were subsequently pelleted at the O.H. Kruse Feed Technology Innovation Center at Kansas State University, Manhattan, KS.

Table 1.

Experiment 1 phases 1 and 2 diet composition (as fed basis)1

CaCO3, %
Item, % 0 0.45 0.90 1.35 1.80 Phase 23
Ingredient
 Corn2 44.07 43.62 43.17 42.72 42.27 48.57
 Soybean meal, 46.5% CP 17.65 17.65 17.65 17.65 17.65 23.73
 Spray-dried whey 10.00 10.00 10.00 10.00 10.00 –
 Whey permeate 10.00 10.00 10.00 10.00 10.00 10.00
 Corn DDGS 5.00 5.00 5.00 5.00 5.00 7.50
 ESBM4 5.00 5.00 5.00 5.00 5.00 5.00
 Menhaden fish meal 2.50 2.50 2.50 2.50 2.50 –
 Spray-dried bovine plasma 2.00 2.00 2.00 2.00 2.00 –
 Choice white grease 1.00 1.00 1.00 1.00 1.00 1.00
 Monocalcium P, 21.5% P 0.80 0.80 0.80 0.80 0.80 1.00
 CaCO3 – 0.45 0.90 1.35 1.80 0.90
 Zinc oxide 0.40 0.40 0.40 0.40 0.40 0.25
 Sodium chloride 0.30 0.30 0.30 0.30 0.30 0.50
 Vitamin premix with phytase5 0.25 0.25 0.25 0.25 0.25 0.25
 Trace mineral premix 0.15 0.15 0.15 0.15 0.15 0.15
 L-Lys-HCL 0.40 0.40 0.40 0.40 0.40 0.55
 DL-Met 0.19 0.19 0.19 0.19 0.19 0.22
 L-Thr 0.18 0.18 0.18 0.18 0.18 0.23
 L-Trp 0.03 0.03 0.03 0.03 0.03 0.04
 L-Val 0.09 0.09 0.09 0.09 0.09 0.13
Total 100 100 100 100 100 100
Calculated analysis
SID amino acids, %
 Lys 1.35 1.35 1.35 1.35 1.35 1.35
 Ile:Lys 56 56 56 56 56 55
 Leu:Lys 118 118 118 118 117 116
 Met:Lys 36 36 36 36 36 37
 Met & cys:Lys 58 58 58 58 58 57
 Thr:Lys 64 64 64 64 64 63
 Trp:Lys 19.3 19.3 19.3 19.3 19.3 19.3
 Val:Lys 70 70 70 70 70 70
Total Lys, % 1.51 1.51 1.51 1.52 1.52 1.51
NE, kcal/kg 2,558 2,545 2,534 2,520 2507 2,494
SID Lys:NE, g/Mcal 6.03 6.00 5.97 5.95 5.92 6.26
CP, % 21.5 21.5 21.4 21.4 21.4 21.4
Ca, % 0.49 0.66 0.84 1.01 1.18 0.72
P, % 0.68 0.68 0.68 0.68 0.68 0.63
STTD P, % 0.58 0.58 0.58 0.58 0.58 0.48
Formulated Ca:P 0.72 0.97 1.23 1.48 1.74 1.21
Ca:STTD P 0.84 1.13 1.45 1.74 2.03 1.50
ABC-46 424 481 539 597 655 475
Chemical analysis7
 DM, % 91.4 91.4 91.5 91.5 91.5 –
 CP,% 19.9 19.8 19.7 20.8 20.2 –
 Ash, % 6.1 6.5 7.0 7.5 7.9 –
 Ca, % 0.61 0.80 0.99 1.15 1.37 0.89
 P, % 0.75 0.75 0.77 0.70 0.71 0.60
 ABC-4, mEq/kg8 318 347 376 368 409 –
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1Phase 1 experimental diets were fed from 5.9 to 8 kg.

2Corn level altered with increasing CaCO3 inclusions.

3A common diet was fed following the experimental period.

4HP 300, Hamlet Protein, Findlay, Ohio.

5Ronozyme HiPhos 2700 (DSM Nutritional Products) provided a 0.13 release of STTD P % for 750 FYT/kg inclusion in the diet.

6ABC-4 was calculated based on published ingredient values (Lawlor et al., 2005).

7Three representative samples were collected from each treatment diet and two representative samples were collected from the phase 2 diet, ground with a food processor, and submitted for analysis to the Kansas State University Soil Testing Laboratory for Ca and P analysis. ABC-4 analysis was performed as described by Lawlor et al. (2005).

8ABC-4 was measured and calculated as the amount of acid in milli-equivalents required to bring 1.0 kg of ground feed to a pH of 4.0.

Experiment 2.

A total of 360 castrated male pigs (DNA Line 200 × 400, Columbus, NE; initially 6.2 ± 0.03 kg) were used in a 38 d study with 5 pigs per pen and 12 replications (pens) per treatment. Upon arrival to the nursery research facility, pigs were randomly assigned to pens and then pens were allotted to 1 of 6 dietary treatments. Dietary treatments were formulated like experiment 1 (Tables 2 and 3) and fed in three phases with treatment diets fed from days 0 to 10 (phase 1) and days 10 to 24 (phase 2) with a common phase 3 diet fed from days 24 to 38. Dietary treatments were formulated to provide 0.45%, 0.90%, or 1.35% added CaCO3 with or without 0.5% benzoic acid (VevoVitall, DSM Nutritional Products) added at the expense of ground corn. In phase 1, the calculated dietary Ca levels were 0.66%, 0.83%, and 1.01% with corresponding dietary ABC-4 values of 450, 508, and 566 mEq/kg, respectively, without benzoic acid included. In phase 2, the calculated dietary Ca levels were 0.54%, 0.72%, and 0.89% (387, 445, and 502 mEq/kg of ABC-4 without benzoic acid, respectively). The addition of benzoic acid decreased ABC-4 by approximately 30 mEq/kg when added to the phases 1 and 2 diets. Similar to experiment 1, standard total tract digestibility phosphorus (STTD P) was formulated to exceed requirement estimates so not to be limiting because of high Ca concentrations. A single base diet was manufactured at Hubbard Feeds and packaged in 22.7 kg bags and then transported to Manhattan, KS. Calcium carbonate, benzoic acid, and corn additions were then mixed at the O.H. Kruse Feed Technology Innovation Center at Kansas State University. All treatment diets in experiment 2 were fed in meal form.

Table 2.

Experiment 2 phase 1 diet composition (as-fed basis)1

Benzoic acid2: Without With
Ingredient, % CaCO3, %: 0.45 0.90 1.35 0.45 0.90 1.35
 Corn 44.82 44.30 43.79 44.33 43.84 43.36
 Soybean meal, 46.5% CP 17.47 17.55 17.60 17.47 17.50 17.54
 Spray-dried whey 10.00 10.00 10.00 10.00 10.00 10.00
 Whey permeate 10.00 10.00 10.00 10.00 10.00 10.00
 Corn DDGS 5.00 5.00 5.00 5.00 5.00 5.00
 Fermented soybean meal3 4.00 4.00 4.00 4.00 4.00 4.00
 Menhaden fish meal 2.50 2.50 2.50 2.50 2.50 2.50
 Spray-dried bovine plasma 2.00 2.00 2.00 2.00 2.00 2.50
 Choice white grease 1.00 1.00 1.00 1.00 1.00 1.00
 Monocalcium P 21.5% P 0.80 0.80 0.80 0.80 0.80 1.00
 CaCO3 0.45 0.90 1.35 0.45 0.90 1.35
 Zinc oxide 0.40 0.40 0.40 0.40 0.40 0.40
 Sodium chloride 0.30 0.30 0.30 0.30 0.30 0.30
 Vitamin premix with phytase4 0.25 0.25 0.25 0.25 0.25 0.25
 Trace mineral premix 0.15 0.15 0.15 0.15 0.15 0.15
 L-Lys-HCl 0.40 0.40 0.40 0.40 0.40 0.40
 DL-Met 0.19 0.19 0.19 0.19 0.19 0.19
 L-Thr 0.17 0.17 0.17 0.17 0.17 0.17
 L-Trp 0.02 0.02 0.02 0.02 0.02 0.02
 L-Val 0.08 0.08 0.08 0.08 0.08 0.08
 Benzoic acid – – – 0.50 0.50 0.50
Total 100 100 100 100 100 100
Calculated analysis
SID amino acids, %
 Lys 1.35 1.35 1.35 1.35 1.35 1.35
 Ile:Lys 57 57 57 57 57 57
 Leu:Lys 120 120 119 120 119 119
 Met:Lys 36 36 36 36 36 36
 Met & cys:Lys 59 59 59 59 59 59
 Thr:Lys 64 64 64 64 64 64
 Trp:Lys 19.2 19.2 19.2 19.2 19.2 19.2
 Val:Lys 70 70 70 70 70 70
Total Lys, % 1.51 1.52 1.52 1.51 1.51 1.51
NE, kcal/kg 2,542 2,529 2,518 2,529 2,516 2,505
SID Lys:NE g/Mcal 5.87 5.91 5.94 5.90 5.93 5.96
CP, % 21.5 21.5 21.5 21.5 21.4 21.4
Ca, % 0.66 0.83 1.00 0.66 0.83 1.00
P, % 0.66 0.66 0.66 0.66 0.66 0.66
STTD P, % 0.58 0.58 0.58 0.58 0.58 0.58
Formulated Ca:P 0.99 1.26 1.52 1.00 1.26 1.53
Ca:STTD P 1.14 1.43 1.72 1.14 1.43 1.72
ABC-4, mEq/kg5 450 508 566 420 477 535
Chemical analysis, %6
 DM, % 90.5 90.7 91.0 90.8 90.9 90.4
 CP, % 20.1 20.3 19.8 20.6 20.7 20.6
 Ash, % 6.8 6.9 6.9 6.6 6.9 7.1
 Ca 0.77 0.90 1.04 0.74 0.89 1.05
 P 0.68 0.65 0.63 0.63 0.65 0.58
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1Phase 1 experimental diets were fed for 10 days.

2VevoVitall, DSM Nutritional Products.

3ME Pro, Prairie Aquatech, Brookings, SD.

4Ronozyme HiPhos 2700 (DSM Nutritional Products) provided a 0.12 release of STTD P % for 1250 FYT/kg inclusion in the diet.

5(ABC-4 was calculated based on published or estimated ingredient values (Lawlor et al., 2005).

6Three representative samples were collected from each treatment diet, ground with a food processor, and submitted for analysis to the Kansas State University Soil Testing Laboratory.

Table 3.

Experiment 2 phases 2 and 3 diet composition (as-fed basis)1

Benzoic acid2: Without With
Ingredient, % CaCO3, %: 0.45 0.90 1.35 0.45 0.90 1.35 Phase 33
 Corn 50.16 49.67 49.19 49.62 49.13 48.65 64.71
 Soybean meal, 46.5% CP 23.75 23.79 23.82 23.79 23.83 23.86 31.30
 Whey permeate 10.00 10.00 10.00 10.00 10.00 10.00 –
 Corn DDGS 7.50 7.50 7.50 7.50 7.50 7.50 –
 Fermented soybean meal4 3.85 3.85 3.85 3.85 3.85 3.85 –
 Choice white grease 1.00 1.00 1.00 1.00 1.00 1.00 –
 Monocalcium P, 21.5% P 1.00 1.00 1.00 1.00 1.00 1.00 1.00
 CaCO3 0.45 0.90 1.35 0.45 0.90 1.35 0.85
 Zinc oxide 0.25 0.25 0.25 0.25 0.25 0.25 –
 Sodium chloride 0.50 0.50 0.50 0.50 0.50 0.50 0.60
 Vitamin premix with phytase5 0.25 0.25 0.25 0.25 0.25 0.25 0.25
 Trace mineral premix 0.15 0.15 0.15 0.15 0.15 0.15 0.15
 L-Lys-HCL 0.55 0.55 0.55 0.55 0.55 0.55 0.52
 DL-Met 0.22 0.22 0.22 0.22 0.22 0.22 0.23
 L-Thr 0.22 0.22 0.22 0.22 0.22 0.22 0.22
 L-Trp 0.04 0.04 0.04 0.04 0.04 0.04 –
 L-Val 0.12 0.12 0.12 0.12 0.12 0.12 0.06
 Benzoic acid – – – 0.50 0.50 0.50 –
Total 100 100 100 100 100 100 100
Calculated analysis
SID amino acids, %
 Lys 1.35 1.35 1.35 1.35 1.35 1.35 1.35
 Ile:Lys 56 56 56 56 56 56 55
 Leu:Lys 118 118 118 118 118 118 114
 Met:Lys 37 37 37 37 37 37 37
 Met & cys:Lys 58 58 58 58 58 58 58
 Thr:Lys 63 63 63 63 63 63 63
 Trp:Lys 19.3 19.3 19.3 19.3 19.3 19.3 20.3
 Val:Lys 70 70 70 70 70 70 69
Total Lys, % 1.51 1.51 1.51 1.51 1.51 1.51 1.49
NE, kcal/kg 2,503 2,489 2,476 2,487 2,476 2,463 2,423
SID Lys:NE, g/Mcal 6.14 6.17 6.20 6.17 6.21 6.24 5.67
CP, % 21.5 21.4 21.4 21.4 21.4 21.4 21.2
Ca, % 0.54 0.72 0.89 0.54 0.72 0.89 0.68
P, % 0.61 0.61 0.61 0.61 0.61 0.60 0.61
STTD P, % 0.51 0.51 0.51 0.51 0.51 0.51 0.47
Formulated Ca:P 0.89 1.18 1.47 0.89 1.18 1.47 1.13
Ca:STTD P 1.06 1.41 1.75 1.06 1.41 1.75 1.45
ABC—4, mEq/kg6 387 445 502 357 415 473 412
Chemical analysis, %7
 DM 89.9 90.2 90.4 90.0 89.9 90.2 –
 CP, % 19.7 18.7 19.0 18.9 20.5 19.3 –
 Ash, % 5.2 6.2 7.2 5.4 5.8 6.0 –
 Ca 0.58 0.74 1.04 0.61 0.79 1.07 –
 P 0.52 0.51 0.53 0.58 0.59 0.54 –
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1Phase 2 experimental diets were fed from days 10 to 24.

2VevoVitall, DSM Nutritional Products.

3Phase 3 common diet was fed from days 24 to 38.

4ME Pro, Prairie Aquatech.

5Ronozyme 2700 (DSM Nutritional Products) provided a 0.13 release of STTD P % for 1250 FYT/kg inclusion in the diet.

6ABC-4 was calculated based on published or estimated ingredient values (Lawlor et al., 2005).

7Three representative samples were collected from each treatment diet, ground with a food processor, and submitted for analysis to the Kansas State University Soil Testing Laboratory.

Data Collection

Pigs were weighed individually, and feed disappearance was measured for each pen on days 0, 14, and 28 in experiment 1, and on days 0, 10, 24, and 38 in experiment 2 to determine average daily gain (ADG), average daily feed intake (ADFI), and gain-to-feed ratio (G:F). On day 10 of experiment 1 and on day 7 of experiment 2, ~40 g of feces were pooled from 3 randomly selected pigs per pen and then dried at 55 °C for 48 h to determine fecal DM. On day 21 of experiment 2, blood was collected from the jugular region of 1 randomly selected pig per pen (72 pigs; 12 observations per treatment), centrifuged at 4 °C and 1800 × g for 30 min, and 1.0 mL serum collected.

Diet Sampling and Chemical Analysis

In both experiments, complete diet samples of each treatment were taken with a grain probe from every other bag (phase 1) and every third bag (phase 2) upon completion of manufacturing. Samples were combined to obtain a homogenous sample of each diet and were stored at −20 °C until further analysis.

Six subsamples of each diet were collected by using a riffle splitter and ground with a food processor to create a homogeneous sample. After creating these homogenous samples, three subsamples were submitted to the K-State Research and Extension Soil Testing Laboratory in Manhattan, KS, for analysis of Ca (AOAC 985.01, 2006) and P (AOAC 985.01, 2006). In experiment 1, ABC-4 was determined as described by Lawlor et al. (2005). In experiment 2, 0.5 mL of serum was submitted to the Kansas State University Veterinary Diagnostics Laboratory for analysis of Ca and P (Cobas c 501, Roche Diagnostics).

Statistical Analysis

In experiment 1, data were analyzed as a randomized complete block design with pen serving as the experimental unit. Treatment was included in the statistical model as a fixed effect, and block was incorporated in the model as a random intercept to account for initial pen average body weight, barn, and group (groups 1 and 2). In experiment 2, data were analyzed as a completely randomized design with pen serving as the experimental unit. Treatment was included in the statistical model as a fixed effect, and barn was incorporated in the model as a random intercept to account for pigs being housed in two identical nursery barns. Data were analyzed using R Studio (Version 3.5.2, R Core Team. Vienna, Austria). Contrasts were used to test for linear and quadratic responses to CaCO3 (experiments 1 and 2) and for the main effects of CaCO3, benzoic acid, and their interaction (experiment 2). Model assumptions including normality were evaluated using visual assessment of studentized residual plots and appeared to be reasonably met. Differences between treatments were considered significant at P ≤ 0.05 and marginally significant at 0.05 < P ≤ 0.10.

RESULTS

The analyzed ABC-4 values of the experimental diets in experiment 1 were lower than calculated (Table 1) however increased with increasing CaCO3 in the diet as expected. Crude protein content was relatively similar across dietary treatments as expected and ash content increased with increasing CaCO3 concentrations (Tables 1, 2, and 3).

Experiment 1

There was no evidence for treatment × group interactions, so data from both groups were combined. From days 0 to 14 (treatment period), ADG (linear, P = 0.010) and day 14 BW (linear, P = 0.006) decreased as CaCO3 increased (Table 4). Likewise, G:F decreased (linear, P < 0.001) as CaCO3 increased with no evidence for difference in ADFI observed. For fecal DM collected on day 10, there was a trend (quadratic, P = 0.091) where pigs fed the highest CaCO3 had the greatest DM where other treatments were relatively similar.

Table 4.

Effects of increasing CaCO3 on weanling pig growth performance, experiment 11

CaCO3, %2 P = 
Item 0.00 0.45 0.90 1.35 1.80 SEM Linear Quadratic
BW, kg
 Day 0 5.9 5.9 5.9 5.9 5.9 0.02 0.846 0.498
 Day 14 8.0 8.0 7.8 7.7 7.7 0.11 0.006 0.641
 Day 28 14.7 14.9 14.8 14.5 14.6 0.23 0.397 0.612
Experimental period (days 0 to 14)
 ADG, g 149 147 136 129 133 7.2 0.010 0.443
 ADFI, g 171 170 170 164 171 7.4 0.676 0.627
 G:F, g/kg 864 854 805 783 776 18.8 < 0.001 0.585
Common period (days 14 to 28)3
 ADG, g 477 489 498 485 494 14.9 0.331 0.470
 ADFI, g 659 682 678 660 669 15.4 0.798 0.424
 G:F, g/kg 723 725 730 734 735 10.4 0.182 0.914
Overall (days 0 to 28)
 ADG, g 312 314 312 304 311 9.7 0.569 0.954
 ADFI, g 413 417 418 408 416 11.1 0.918 0.920
 G:F, g/kg 753 751 745 744 745 7.1 0.246 0.736
Fecal DM, %4
 Day 10 22.5 22.1 21.9 21.5 24.4 1.1 0.303 0.091
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1A total of 695 weanling barrow pigs (DNA 200 × 400; initially 5.9 ± 0.02 kg) approximately 21 d of age were used in two 28-d experiments with 5 pigs per pen and 27 or 28 pens per treatment.

2Analyzed Ca of the treatment diets were 0.61%, 0.80%, 0.99%, 1.15%, and 1.37%, respectively.

3Analyzed Ca of the common phase 2 diet was 0.89%.

4Feces from three pigs from each pen were pooled, weighed, and dried to measure fecal DM.

From days 14 to 28 (common period) and for the overall experiment (days 0 to 28), there was no evidence for differences in growth performance between treatments.

Experiment 2

For all response criteria, there was no evidence for CaCO3 × benzoic acid interactions observed (Table 5). From days 0 to 10, pigs fed benzoic acid tended to have increased (P = 0.092) ADG and had increased (P = 0.042) ADFI (Table 6). From days 10 to 24, pigs fed decreasing CaCO3 had improved (linear, P = 0.022) G:F but ADG, ADFI, and day 24 BW were not influenced by dietary treatment. For the experimental period (days 0 to 24), there was a tendency observed for benzoic acid to improve (P = 0.056) ADG and (P = 0.071) ADFI, and an improvement (linear, P = 0.014) was observed in G:F as CaCO3 decreased in the diet.

Table 5.

Interactive effects of CaCO3 with or without benzoic acid on nursery pig growth performance, fecal DM and blood calcium and phosphorus concentration, experiment 21

P = 
Benzoic acid2: Without With CaCO3 × benzoic acid
Item CaCO3, %: 0.45 0.90 1.35 0.45 0.90 1.35 SEM Linear Quadratic
BW, kg
 Day 0 6.2 6.2 6.2 6.2 6.2 6.2 0.03 0.948 0.636
 Day 10 7.5 7.4 7.5 7.5 7.6 7.6 0.12 0.451 0.534
 Day 24 13.2 13.1 12.9 13.3 13.2 13.4 0.31 0.535 0.784
 Day 38 21.0 20.8 20.8 21.5 21.3 21.5 0.46 0.847 0.871
Phase 1 period (days 0 to 10)
 ADG, g 130 117 128 132 140 146 13.9 0.451 0.471
 ADFI, g 137 132 144 147 146 160 10.4 0.715 0.878
 G:F, g/kg 940 846 855 891 954 913 57.4 0.241 0.188
Phase 2 period (days 10 to 24)
 ADG, g 401 399 385 416 402 410 25.1 0.677 0.446
 ADFI, g 526 530 517 538 526 563 23.4 0.292 0.259
 G:F, g/kg 762 753 743 773 763 729 20.4 0.359 0.657
Experimental period (days 0 to 24)
 ADG, g 287 274 276 297 291 295 12.4 0.655 0.936
 ADFI, g 362 355 359 375 365 387 13.2 0.516 0.602
 G:F, g/kg 791 771 768 793 797 763 11.2 0.751 0.129
Common period (days 24 to 38)
 ADG, g 553 554 562 584 580 581 15.9 0.693 0.966
 ADFI, g 829 829 827 851 840 859 16.7 0.766 0.561
 G:F, g/kg 666 669 679 686 689 676 10.4 0.301 0.513
Overall (days 0 to 38)
 ADG, g 384 373 379 403 396 396 11.7 0.904 0.736
 ADFI, g 531 522 527 550 539 554 13.1 0.736 0.775
 G:F, g/kg 721 714 718 732 736 715 7.6 0.281 0.160
Fecal DM, %3
 Day 7 27.5 30.4 29.8 28.1 27.3 28.3 1.31 0.303 0.159
Serum4
 Ca, mg/Dl 10.7 11.2 11.6 11.0 11.3 11.6 0.21 0.355 0.942
 P, mg/dL 11.0 10.6 11.0 10.9 11.3 10.8 0.32 0.897 0.156
Open in a new tab

1A total of 360 weanling barrows (DNA 200 × 400, initially 6.2 ± 0.03 kg) approximately 21 d of age were used in a 38-d experiment with 5 pigs per pen and 12 pens per treatment.

2DSM Nutritional Products.

3Feces from three pigs from each pen were pooled, weighed, and dried to measure fecal DM.

4Blood was collected from 1 pig per pen on day 21 and submitted to the Kansas State University Veterinary Diagnostic Lab for Ca and P analysis.

Table 6.

Main effects of CaCO3 and benzoic acid on nursery pig growth performance, fecal DM and blood calcium and phosphorus concentrations, experiment 21

CaCO3, %: P =  Benzoic acid2:
Item 0.45 0.90 1.35 SEM Linear Quadratic Without With SEM P = 
BW, kg
 Day 0 6.2 6.2 6.2 0.03 0.793 0.283 6.2 6.2 0.03 0.257
 Day 10 7.5 7.5 7.6 0.10 0.598 0.403 7.4 7.6 0.10 0.156
 Day 24 13.3 13.1 13.2 0.26 0.620 0.665 13.1 13.3 0.23 0.294
 Day 38 21.2 21.1 21.2 0.38 0.821 0.678 20.9 21.4 0.35 0.059
Phase 1 period (days 0 to 10)
 ADG, g 131 129 137 12.0 0.550 0.529 125 139 11.2 0.092
 ADFI, g 142 139 152 8.8 0.228 0.245 138 151 8.2 0.042
 G:F, g/kg 915 900 884 47.9 0.485 0.990 880 919 44.3 0.293
Phase 2 period (days 10 to 24)
 ADG, g 408 400 397 23.4 0.397 0.832 395 409 22.8 0.188
 ADFI, g 532 528 540 20.4 0.595 0.566 524 542 19.4 0.174
 G:F, g/kg 768 758 736 18.1 0.022 0.611 752 755 17.2 0.799
Experimental period (days 0 to 24)
 ADG, g 292 282 286 10.3 0.519 0.451 279 295 9.4 0.056
 ADFI, g 368 360 373 10.5 0.690 0.288 358 376 9.4 0.071
 G:F, g/kg 792 784 766 8.5 0.014 0.595 777 784 7.3 0.374
Common period (days 24 to 38)
 ADG, g 569 567 572 11.7 0.846 0.839 557 582 10.0 0.045
 ADFI, g 840 835 843 12.6 0.849 0.607 828 850 10.9 0.091
 G:F, g/kg 676 679 678 7.3 0.883 0.851 672 684 6.0 0.159
Overall (days 0 to 38)
 ADG, g 393 384 387 9.5 0.531 0.485 378 398 8.7 0.011
 ADFI, g 541 530 541 10.3 0.982 0.288 527 548 9.1 0.030
 G:F, g/kg 726 725 716 5.8 0.163 0.550 718 727 5.1 0.096
Fecal DM, %3
 Day 7 27.8 28.8 29.0 1.09 0.249 0.657 29.2 27.9 1.00 0.126
Serum 4
 Ca, mg/dL 10.8 11.3 11.6 0.15 < 0.01 0.808 11.2 11.3 0.13 0.470
 P, mg/dL 10.9 11.0 10.9 0.23 0.959 0.941 10.9 11.0 0.19 0.591
Open in a new tab

1A total of 360 weanling barrows (DNA 200 × 400, initially 6.2 ± 0.03 kg) approximately 21 d of age were used in a 38-d experiment with 5 pigs per pen and 24 pens per CaCO3 treatment and 36 pens per benzoic acid treatment. There was no CaCO3 × benzoic acid interactions observed (P > 0.10).

2DSM Nutritional Products.

3Feces from three pigs from each pen were pooled, weighed, and dried to measure fecal DM.

4Blood was collected from 1 pig per pen on day 21 and submitted to the Kansas State University Veterinary Diagnostic Lab for Ca and P analysis.

During the common period (days 24 to 38), pigs previously fed benzoic acid had increased (P = 0.045) ADG and marginally increased (P = 0.091) ADFI. For the overall study, pigs fed with benzoic acid had increased ADG (P = 0.011) and ADFI (P = 0.030) and marginally improved G:F (P = 0.096) and final BW (P = 0.059); however, no overall impact of CaCO3 level was observed.

For fecal DM on day 7, there was no evidence for differences among treatments. For serum analysis on day 21, serum Ca increased (linear, P < 0.001) as the level of CaCO3 in the diet increased, while no difference in serum P was observed.

DISCUSSION

Calcium (Ca) is one of the most abundant macrominerals required by the pig and 0.8% of the animals’ body is Ca (Hendriks and Moughan, 1993). Of that 0.8%, 96% to 99% is present in bone tissue in the form of hydroxyapatite. Calcium is therefore essential for bone formation and mineralization. In the present study, a reduction of calcium carbonate was used to decrease the ABC-4 of the diet and as a consequence, the total dietary Ca percentage decreased. However, the analyzed Ca values were higher than the calculated values and revealed that the pigs fed the diets at or below 0.45% CaCO3 in both experiments and the 0.90% CaCO3 in experiment 2 were below the NRC (2012) requirement estimates of 0.85% and 0.80% for 5 to 7 kg and 7 to 11 kg, respectively. However, if providing a 0.10% Ca release value for phytase inclusion, only the diet with no CaCO3 used in experiment 1 was Ca deficient. It can be assumed that difference in analyzed Ca is due to a discrepancy in a Ca concentration of one or more ingredients used in the experiments and/or analytical error. As well, analyzed ABC-4 values were lower than the calculated values and could be attributed to variation in the ingredient values compared to those provided from Lawlor et al. (2005).

In the present study the Ca:P ratio increased as the concentration of CaCO3 increased. The Ca:P ratio appears to be more critical to growth performance and bone mineralization at low P levels (Wu et al., 2018). Qian et al. (1996) observed decreased ADG when Ca:P increased from 1.2:1 to 2:1. This response was greater when diets were fed with deficient P levels. To avoid this concern, dietary STTD P in the present experiments were at least 0.58%, which is much greater than NRC (2012) requirement estimates of 0.45% and 0.40% for pigs weighing 5 to 7 and 7 to 11 kg, respectively. Wu et al. (2018) observed interactive effects of dietary Ca and P in the first 24 d of the nursery period. They observed increasing Ca by increasing CaCO3 significantly reduced G:F in diets fed at the NRC (2012) requirement estimate (0.45% STTD P) for 5 to 7 kg pigs, but no difference compared to the diets that were fed above the requirement estimate (0.56% STTD P). These data altogether show that pigs fed with adequate dietary P can maintain performance when fed with a wide range of Ca levels. Thus, improvements in performance when nursery pigs were fed lower Ca levels may be a result of reduced diet ABC-4.

The use of ABC-4 has been evaluated more extensively in European nursery diets (Blank et al., 1999; Mroz et al., 2000; Lawlor et al., 2006) compared to US-based formulations. Lawlor et al. (2005) conducted acid/base titrations to develop ABC-4 ingredient values that were used in diet formulation in the present study. With the purpose of evaluating ABC-4 diet values on growth performance, Lawlor et al. (2006) fed different Ca and P levels with and without acidifiers. They observed that low Ca (0.28%) and P (0.51%) concentrations for the first 7 d postweaning improved ADFI and tended to improve feed conversion through the first 14 d. The improvement in feed conversion they found agrees with the present experiments. The change in Ca investigated by Lawlor et al. (2006) was completed by removing limestone flour (1.2%) and dicalcium phosphate (1.0%), ultimately lowering ABC-4 values from 315 to 207 mEq/kg. In a separate experiment, Lawlor et al. (2006) observed no growth response to diet Ca level when feeding limestone flour from 0.03% to 1.19% (340 to 500 mEq/kg ABC-4) of the diet while maintaining constant total P. Finally, Lawlor et al. (2006) also examined keeping limestone flour and dicalcium phosphate constant and included 2.0% formic acid, which lowered the ABC-4 from 315 to 180 mEq/kg. They reported a mineral level × acid interaction with increased ADFI when pigs were fed formic acid with adequate (NRC, 1998) Ca and P in the first 7 d, but no difference when formic acid was fed with low Ca and P levels. This interaction is in contrast with the present study, where no interaction was found between acid and Ca level, which could be attributed to the type or level of acidifier used or other ingredient combinations that made up the experimental diets.

Given the NRC (2012) requirement estimates of 0.85% and 0.80% Ca for pigs weighing 5 to 7 kg and 7 to 11 kg, respectively, the pigs in the present studies fed the low CaCO3 levels were deficient in Ca on a calculated basis (≤ 0.66% and 0.72% in experiments 1 and 2, respectively). However, diet Ca values from chemical analysis revealed that only the 0% added CaCO3 diets were below while the 0.45% were only slightly below the NRC (2012) requirement estimates. Also, all diets contained added phytase which is shown to increase Ca availability. These calculations were not considered in the present studies, and therefore, even the diet without CaCO3 would most likely been at or very close to the pigs Ca requirement.

The concern of feeding below the pig’s Ca requirement for an extended period is that bone mineralization would likely be limited. This is supported by Lagos et al. (2021) who fed weaned pigs’ diets with 50% (NRC, 2012) estimated Ca and P levels for 16 d. These authors reported decreased bone mineralization at day 15 with no differences in the growth performance. While we did not measure bone mineralization directly, in experiment 2 there were statistical differences for serum Ca with serum Ca percentage decreasing as the level of dietary CaCO3 decreased. However, the serum Ca levels for all treatments were within normal biological ranges 9 to 13 mg/dL (Puls, 1994). The response to serum Ca being reflective of diet Ca concentration agrees with previous studies (Nielsen et al., 1971; Mahan, 1982; Hall et al., 1991; Lagos et al., 2019). We hypothesize that the short-term reduction in Ca concentrations by removing CaCO3 might only marginally affect bone mineralization, but the benefits of low CaCO3 on growth performance by either decreasing ABC-4, or a response to less mineral in the diet on net energy (NE) concentration would out-weigh this potential transitory effect on bone mineralization. However, further research on the impacts of bone mineral content should be assessed to confirm our hypothesis.

The use of acidifiers in nursery diets and the proposed mechanism of action has been extensively researched and reviewed (Kim et al., 2005; Kil et al., 2011; Suiryanrayna and Ramana, 2015). Acidifiers added to feeds are used to decrease stomach and lower GIT pH, improve nutrient digestibility, and decrease pathogen proliferation. A low stomach pH is required for adequate protein digestion because pepsinogen is more rapidly cleaved to produce pepsin at a pH 2.5 to 3.0 (Herriott, 1938). Pepsin is the primary proteolytic enzyme of the stomach. Although it was not the objective of this study to measure gastric pH, numerical changes in stomach pH with different acidifiers has been researched (Kil et al., 2011) where it was reported that statistical differences of stomach pH are variable due to other dietary ingredient additions with varying ABC-4 estimates. Certain ingredients with high ABC-4 may interact with acidifiers to lessen their response. Although we did not see an interaction between calcium carbonate and benzoic acid in the present study, an interaction with other ingredients or a combination of ingredients that have relatively high ABC-4 values may exist, but this would require further investigation.

In the present study, it was hypothesized that an acidifier would further decrease the ABC-4 of the diet and potentially provide additional benefit regardless of CaCO3 level in the diet. Therefore, benzoic acid was used due to previous research evaluating early nursery diets where improvements in growth performance and nutrient utilization have been shown (Guggenbuhl et al., 2007; Chen et al., 2017; Diao et al., 2021). Guggenbuhl et al. (2007) compared feeding 0.50% benzoic acid to a control diet and observed increased total digestibility of nitrogen, energy, and apparent ileal digestibility of Lys and Thr. Although it was not measured, the improvement of ADG and ADFI when benzoic acid was fed in the present study might be attributed to an increase in nutrient digestibility. The inclusion of benzoic acid in the present study decreased the calculated ABC-4 by 30 mEq/kg. It is unclear whether the magnitude was sufficient to illicit a statistical growth response that could be attributed to lower ABC-4.

In our diet formulation, CaCO3 and benzoic acid were added at the expense of ground corn, and as a result the dietary energy decreased in these diets. Decreasing the dietary NE by 1% has been shown to decrease G:F by 1% (Nitikanchana et al., 2015). It was therefore expected in the present study that we could observe reductions in G:F as CaCO3 increased in the diet. However, in experiment 1 increasing CaCO3 from 0% to 1.80% reduced diet NE by 2%, while we observed a 10% reduction in G:F when the experimental diets were fed. Similarly, in experiment 2, increasing CaCO3 reduced NE by 0.9% and 1% in phases 1 and 2, respectively, and yet we observed a 3% reduction in G:F when treatment diets were fed. From these observations, we can conclude that the change in G:F may not be solely attributed to dietary NE.

In summary, increasing CaCO3 in the early nursery diets with adequate dietary P decreased BW, ADG, and G:F. This response is potentially due to the increase in the ABC-4 of the diet or change in NE concentration. The use of benzoic acid showed an improvement in ADG and ADFI and marginal improvement in G:F, and the response was independent of the dietary CaCO3. While not unexpected, serum Ca level decreased with reduced diet Ca levels. Additional research needs to be conducted to determine if the results were a direct result of changes in ABC-4 from altering the diet CaCO3 concentration or other mechanisms.

ACKNOWLEDGMENTS

Contribution No. 23-301-J from the Kansas Agricultural Experiment Station.

Glossary

Abbreviations:

ABC-4

acid binding capacity

ADFI

average daily feed intake;

ADG

average daily gain;

BW

body weight

Ca:P

calcium-to-phosphorus ratio;

CaCO3

calcium carbonate;

CP

crude protein;

DDGS

dried distillers grains with solubles;

DM

dry matter;

ESBM

enzymatically treated soybean meal;

FYT

phytase unit;

G:F

gain-to-feed;

GIT

gastrointestinal tract;

NE

net energy;

SID

standardized ileal digestibility;

STTD

standard total tract digestibility

Contributor Information

Alan J Warner, Department of Animal Sciences and Industry, College of Agriculture, Kansas State University, Manhattan, KS 66506-0201, USA.

Joel M DeRouchey, Department of Animal Sciences and Industry, College of Agriculture, Kansas State University, Manhattan, KS 66506-0201, USA.

Mike D Tokach, Department of Animal Sciences and Industry, College of Agriculture, Kansas State University, Manhattan, KS 66506-0201, USA.

Jason C Woodworth, Department of Animal Sciences and Industry, College of Agriculture, Kansas State University, Manhattan, KS 66506-0201, USA.

Robert D Goodband, Department of Animal Sciences and Industry, College of Agriculture, Kansas State University, Manhattan, KS 66506-0201, USA.

Jordan T Gebhardt, Department of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506-0201, USA.

Conflict of interest statement

None declared.

LITERATURE CITED

  1. AOAC. 2006. Official methods of analysis AOAC international. 18th ed. Arlington, VA: Association of Official Analytical Chemists. [Google Scholar]
  2. Bergstrom, J., Landero J., Young M., and Hahn J. D.. . 2020. The effects of pure benzoic acid, and acid blend product, or their combination in nursery pig diets on postweaning growth performance. J. Anim. Sci. 98(Suppl.3):80–81 (Abstr.). doi: 10.1093/jas/skaa054.144 [DOI] [Google Scholar]
  3. Blank, R., Mosenthin R., Sauer W. C., and Huang S.. . 1999. Effect of fumaric acid and dietary buffering capacity on ileal and fecal amino acid digestibilities in early weaned pigs. J. Anim. Sci. 77:2974–2984. doi: 10.2527/1999.77112974x [DOI] [PubMed] [Google Scholar]
  4. Bradley, C. L., Bergstrom J., Nemechek J., and Hahn J. D.. . 2020. The effects of adding two organic acid blends with or without high levels of zinc or copper, on postweaning pig performance. J. Anim. Sci. 98(Suppl.3):209–210 (Abstr.). doi: 10.1093/jas/skaa054.362 [DOI] [Google Scholar]
  5. Chen, J. L., Zheng P., Zhang C., Yu B., He J., Yu J., Luo J. Q., Mao X. B., Huang Z. Q., and Chen D. W.. . 2017. Benzoic acid beneficially affects growth performance of weaned pigs which was associated with changes in gut bacterial populations, morphology indices and growth factor gene expression. J. Anim. Physiol. Anim. Nutr. 101:1137–1146. doi: 10.1111/jpn.12627 [DOI] [PubMed] [Google Scholar]
  6. Crenshaw, T. D. 2001. Calcium, phosphorus, vitamin D and vitamin K in swine nutrition. In: Lewis, A. J., and Southern L. L., editors. Swine nutrition, 2nd ed. Boca Raton, FL: CRC Press; p. 187–212. [Google Scholar]
  7. Diao, H., Zheng P., Yu B., He J., Mao X. B., Yu J., and Chen D. W.. . 2021. Corrigendum to ‘Effects of dietary supplementation with benzoic acid on intestinal morphological structure and microflora in weaned piglets’. Livest. Sci. 254:104737. doi: 10.1016/j.livsci.2014.05.029 [DOI] [Google Scholar]
  8. Guggenbuhl, P., Séon A., Piñón Quintana A., and Simões Nunes C.. . 2007. Effects of dietary supplementation with benzoic acid (VevoVitall) on the zootechnical performance, the gastrointestinal microflora and ileal digestibility of the young pig. Livest. Sci. 108:218–221. doi: 10.1016/j.livsci.2007.01.068 [DOI] [Google Scholar]
  9. Halas, D., Hansen C. F., Hampson D. J., Mullan B. P., Kim J. C., Wilson R. H., and Pluske J. R.. . 2010. Dietary supplementation with benzoic acid improves apparent ileal digestibility of total nitrogen and increases villous height and caecal microbial diversity in weaner piglets. Anim. Feed Sci. Technol. 160:137–147. doi: 10.1016/j.anifeedsci.2010.07.001 [DOI] [Google Scholar]
  10. Hall, D. D., Cromwell G. L., and Stahly T. S.. . 1991. Effects of dietary calcium, phosphorus, calcium:phosphorus ratio and vitamin K on performance, bone strength, and blood clotting status of pigs. J. Anim. Sci. 69:646–655. doi: 10.2527/1991.692646x [DOI] [PubMed] [Google Scholar]
  11. Hendriks, W. H., and Moughan P. J.. . 1993. Whole-body mineral ­composition of entire male and female pigs depositing protein at maximal rates. J. Livest. Prod. Sci. 33:161–170. doi: 10.1016/0301-6226(93)90247-F [DOI] [Google Scholar]
  12. Herriott, R. M. 1938. Kinetics of the formation of pepsin from swine pepsinogen and identification of an intermediate compound. J. Gen. Physiol. 22:65–78. doi: 10.1085/jgp.22.1.65 [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jasaitis, D. K., Wohlt J. E., and Evans J. L.. . 1987. Influence of feed-ion content on buffering capacity of ruminant feedstuffs in-vitro. J. Dairy Sci. 70:1391–1403. doi: 10.3168/jds.S0022-0302(87)80161-3 [DOI] [Google Scholar]
  14. Kil, D. Y., Kwon W. B., and Kim B. G.. . 2011. Dietary acidifiers in weanling pigs diets: a review. Rev. Colomb. Cienc. 24:231–247. [Google Scholar]
  15. Kim, Y. Y., Kil D. Y., Oh H. K., and Han I. K.. . 2005. Acidifier as an alternative material to antibiotics in animal feed. Asian-Aust. J. Anim. Sci. 18:1048–1060. doi: 10.5713/ajas.2005.1048 [DOI] [Google Scholar]
  16. Kluge, H., Broz J., and Eder K.. . 2006. Effect of benzoic acid on growth performance, nutrient digestibility, nitrogen balance, ­gastrointestinal microflora and parameters of microbial metabolism in piglets. J. Anim. Physiol. Anim. Nutr. 90:316–324. doi: 10.1111/j.1439-0396.2005.00604.x [DOI] [PubMed] [Google Scholar]
  17. Lagos, L. V., Lee S. A., Fondevila G., Walk C. L., Murphy M. R., Loor J. J., and Stein H. H.. . 2019. Influence of the concentration of dietary digestible calcium on growth performance, bone mineralization, plasma calcium, and abundance of genes involved in intestinal absorption of calcium in pigs from 11 to 22 kg fed diets with different concentrations of digestible phosphorus. J. Anim. Sci. Biotechnol. 10:47. doi: 10.1186/s40104-019-0349-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lagos, L. V., Lee S. A., Bedford M. R., and Stein H. H.. . 2021. Reduced concentrations of limestone and monocalcium phosphate in diets without or with microbial phytase did not influence gastric pH, fecal score, or growth performance, but reduced bone ash and serum albumin in weanling pigs. Transl. Anim. Sci. 5:1–10. doi: 10.1093/tas/txab115 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lawlor, P. G., Lynch P. B., and Caffrey P. J.. . 2006. Effects of fumaric acid, calcium formate and mineral levels in diets on the intake and growth performance of newly weaned pigs. Irish. J. Agr. Food. Res. 45:61–71. https://www.jstor.org/stable/25562563 [Google Scholar]
  20. Lawlor, P. G., Lynch P. B., Caffrey P. J., O’Reilly J. J., and O’Connell M. K.. . 2005. Measurements of the acid binding capacity of ingredients used in pig diets. Ir. Vet. J. 58:447–452. doi: 10.1186/2046-0481-58-8-447 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Li, Z., Yi G., Yin J., Sun P., Li D., and Knight C.. . 2008. Effects of organic acids on growth performance, gastrointestinal pH, intestinal microbial populations, and immune responses of weaned pigs. Asian-Aust. J. Anim. Sci. 21:252–261. doi: 10.5713/ajas.2008.70089 [DOI] [Google Scholar]
  22. Mahan, D. C. 1982. Dietary calcium and phosphorus levels for weanling swine. J. Anim. Sci. 54:559–564. doi: 10.2527/jas1982.543559x [DOI] [PubMed] [Google Scholar]
  23. Mroz, Z., Jongbloed A. W., Partanene K. H., Vreman K., Kemme P. A., and Kogut J.. . 2000. The effects of calcium benzoate in diets with or without organic acids on the buffering capacity, apparent digestibility, retention of nutrients, and manure characteristics in swine. J. Anim. Sci. 78:2622–2632. doi: 10.2527/2000.78102622x [DOI] [PubMed] [Google Scholar]
  24. Nielsen, N. C., Andersen S., Madsen A., and Mortensen H. P.. . 1971. Dietary calcium-phosphorus ratios for growing pigs in relation to serum levels and bone development. Acta Vet. Scand. 12:202–219. doi: 10.1186/BF03547753 [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nitikanchana, S., Dritz S. S., Tokach M. D., DeRouchey J. M., Goodband R. D., and White B. J.. . 2015. Regression analysis to predict growth performance from dietary net energy in growing-finishing pigs. J. Anim. Sci. 93:2826–2839. doi: 10.2527/jas.2015-9005 [DOI] [PubMed] [Google Scholar]
  26. NRC. 1998. Nutrient requirements of swine. 9th ed. Washington, DC: National Academy Press. [Google Scholar]
  27. NRC. 2012. Nutrient requirements of swine. 11th rev. ed. Washington (DC): National Academic Press. [Google Scholar]
  28. Puls, R. 1994. Vitamins in animal health. Clearbrook, BC. Canada: Sherpa International. [Google Scholar]
  29. Qian, H., Kornegay E. T., and D. E.Conner, Jr. 1996. Adverse effects of wide calcium:phosphorus ratios on supplemental phytase efficacy for weanling pigs fed two dietary phosphorus levels. J. Anim. Sci. 74:1288–1297. doi: 10.2527/1996.7461288x [DOI] [PubMed] [Google Scholar]
  30. Smith, H. W., and Jones J. E. T.. . 1963. Observations on the alimentary tract and its bacterial flora in healthy and diseased pigs. J. Pathol. Bacteriol. 86:387–412. doi: 10.1002/path.1700860214 [DOI] [PubMed] [Google Scholar]
  31. Suiryanrayna, M. V. A. N., and Ramana J. V.. . 2015. A review of the effects of dietary organic acids fed to swine. J. Anim. Sci. Biotechnol. 6:45. doi: 10.1186/s40104-015-0042-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wu, F., Tokach M. D., Dritz S. S., Woodworth J. C., DeRouchey J. M., Goodband R. D., Gonçalves M. A. D., and Bergstrom J. R.. . 2018. Effects of dietary calcium to phosphorus ratio and addition of phytase on growth performance of nursery pigs. J. Anim. Sci. 96:1825–1837. doi: 10.1093/jas/sky101 [DOI] [PMC free article] [PubMed] [Google Scholar]

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