Comparative amino acid digestibility between broiler chickens and pigs fed different poultry by-products and meat and bone meal

Abstract

The objective of this study was to compare the standardized ileal digestibility (SID) of amino acids (AA) in 3 poultry by-products including hydrolyzed feather meal (HFM), flash dried poultry protein (FDPP), and poultry meal (PM) and also a meat and bone meal (MBM) between broiler chickens and pigs. Experimental diets consisted of 4 diets containing each test ingredient as a sole source of nitrogen and a nitrogen-free diet. In experiment 1, 416 male broiler chickens with a mean initial body weight (BW) of 705 ± 100 g were allotted to 5 diets with 8 replicate cages per diet in a randomized complete block design with BW as a blocking factor at day 18 posthatching. After 5 d of feeding experimental diets, birds were euthanized by CO₂ asphyxiation, and ileal digesta samples were collected from distal two-thirds of the ileum. In experiment 2, 10 barrows with a mean initial BW of 22.1 ± 1.59 kg were surgically fitted with T-cannulas at the distal ileum and allotted to a duplicate 5 × 4 incomplete Latin Square design with 5 diets and 4 periods. Each period lasted for 7 d including 5 d of adaptation and 2 d of ileal digesta collection. Data from experiments 1 and 2 were pooled together and analyzed as a 2 × 4 factorial arrangement with the effects of species (broiler chickens or pigs) and 4 experimental diets (HFM, FDPP, PM, or MBM). There were interactions (P < 0.05) between experimental diets and species in the SID of His, Lys, Thr, Trp, Val, and all dispensable AA except Tyr. In broiler chickens, the SID of Lys in FDPP (73.3%) was greater (P < 0.05) than in HFM (55.7%) but was lower (P < 0.05) than in MBM (86.5%), which was not different from PM (78.7%). In pigs, however, the SID of Lys in FDPP and PM (70.0 and 70.1%, respectively) were greater (P < 0.05) than in HFM (39.0%) but were lower (P < 0.05) than in MBM (79.2%). Broiler chickens fed FDPP and PM had lower (P < 0.05) SID of His, Thr, and Trp than those fed MBM; however, there was no difference in the SID of His, Thr, or Trp among pigs fed FDPP, PM, or MBM. The SID of Val in MBM was greater (P < 0.05) than in the other test ingredients for broiler chickens, but there was no difference in the SID of Val among test ingredients for pigs. Pigs had greater (P < 0.05) SID of Ile and Met than broiler chickens. In conclusion, the pattern of differences in the SID of His, Lys, Thr, Trp, and Val, but not the other indispensable AA, among poultry by-products and MBM were different between broiler chickens and pigs.

Introduction

Broiler chickens and pigs are the primary non-ruminant animals raised for human consumption, and their diets typically contain common feed ingredients such as corn and soybean meal. In non-ruminant animals, most of digestion and absorption of protein and amino acids (AA) occur before digesta flows into the hindgut (Pond et al., 2005). Therefore, the standardized ileal digestibility (SID) of AA has been used to evaluate the digestibility of AA in feed ingredients for both broiler chickens and pigs (Kong and Adeola, 2014). However, differences in physical structure and capacity of digestive organs between broiler chickens and pigs may affect the SID of AA in the same feed ingredients. Park et al. (2017) reported that pigs had greater SID of AA in full-fat soybean, soybean meal, and peanut flour than broiler chickens and that the SID of most AA in soybean meal and peanut flour were greater than in full-fat soybean in both broiler chickens and pigs. On the other hand, another study conducted to compare the SID of AA between broiler chickens and pigs revealed that broiler chickens had greater SID of AA in full-fat canola seeds than pigs, which might be due to the beneficial effects of dietary fiber in full-fat canola seeds on the gizzard of broiler chickens (Park et al., 2019). Therefore, feed ingredient-specific factors may differently affect the SID of AA in broiler chickens and pigs.

By-products of meat production have been used to produce protein-rich feed ingredients for both broiler chickens and pigs. From poultry meat production, feathers separated from carcasses are autoclaved to hydrolyze keratin, which is insoluble and indigestible protein for non-ruminant animals, followed by processing to hydrolyzed feather meal (HFM; Papadopoulos, 1985). Inedible portions from poultry meat processing such as skin, bone, or trimmings are used to produce either flash dried poultry protein (FDPP) or poultry meal (PM), depending on the method of heat processing and proportion of bone. Meat and bone meal (MBM) is produced by mixture of by-products from beef, pork, and poultry processing (Hicks and Verbeek, 2016). Nutrient composition as well as their digestibility in meat by-products are affected by various composition, quality of raw materials, and processing conditions such as pressure and temperature (Hicks and Verbeek, 2016). However, it is unclear that the processing effects of meat by-products on SID of AA are different between broiler chickens and pigs. Therefore, the objective of this study was to compare the SID of AA in HFM, FDPP, PM, and MBM between broiler chickens and pigs.

Materials and Methods

Experimental procedures involving animals were reviewed and approved by the Purdue University Animal Care and Use Committee (West Lafayette, IN).

Ingredients and experimental diets

Three poultry by-products including HFM, FDPP, and PM and MBM (Darling Ingredient Inc., Cold Spring, KY) were obtained and used as test ingredients in the current study (Table 1). Five experimental diets were prepared based on cornstarch and sucrose (Tables 2 and 3). Four experimental diets were formulated to contain each test ingredient as a sole source of nitrogen, providing 160 g/kg crude protein (CP) in each diet. A nitrogen-free diet (NFD) was prepared to estimate the basal ileal endogenous losses (BEL) of CP and AA in both broiler chickens and pigs. Soybean oil and purified cellulose were added into diets as energy and fiber sources, respectively. All diets were prepared to meet or exceed the vitamin and mineral requirement estimates for both broiler chickens and pigs suggested in National Research Council (NRC) for broiler chickens (NRC, 1994) and pigs (NRC, 2012), respectively. Chromic oxide was added at 5 g/kg of diet as an indigestible marker.

Table 1.

Analyzed nutrient composition of HFM, FDPP, PM, and MBM, g/kg as-fed basis

	Ingredient
Item	HFM	FDPP	PM	MBM
Dry matter	958	954	933	965
Gross energy, kcal/kg	5,436	5,105	4,080	4,029
CP1	890	695	500	548
AEE	91	146	159	105
Ash	36	125	290	280
Indispensable AA
Arg	62.9	44.4	33.6	34.9
His	7.2	13.7	7.5	11.0
Ile	41.8	25.9	14.5	14.8
Leu	71.2	45.7	26.2	32.8
Lys	20.1	40.9	24.6	29.0
Met	7.0	13.0	7.9	6.8
Phe	42.8	26.7	16.8	18.9
Thr	41.1	25.5	15.3	16.7
Trp	5.2	6.4	3.0	4.3
Val	69.5	32.3	18.6	23.8
Dispensable AA
Ala	41.7	42.3	35.7	38.7
Asp	59.1	52.9	34.8	39.6
Cys	48.1	8.2	3.4	4.9
Glu	92.1	80.8	56.6	61.6
Gly	70.1	60.3	64.8	67.7
Pro	88.0	40.7	38.4	41.1
Ser	86.3	24.5	14.8	19.0
Tyr	23.6	20.9	10.8	11.4

¹Analyzed nitrogen concentration multiplied by 6.25.

Table 2.

Ingredient composition of experimental diets, g/kg as-fed basis

	Diet
Item	HFM	FDPP	PM	MBM	NFD
Cornstarch	351.2	332.2	243.0	286.0	316.0
Sucrose	300.0	300.0	300.0	300.0	500.0
HFM	181.0	0.0	0.0	0.0	0.0
FDPP	0.0	226.0	0.0	0.0	0.0
PM	0.0	0.0	323.0	0.0	0.0
MBM	0.0	0.0	0.0	280.0	0.0
Soybean oil	50.0	50.0	50.0	50.0	50.0
Cellulose1	50.0	50.0	50.0	50.0	50.0
Ground limestone	12.3	0.8	0.0	0.0	13.0
Monocalcium phosphate	21.5	7.0	0.0	0.0	23.5
Salt	4.0	4.0	4.0	4.0	0.0
Potassium carbonate	0.0	0.0	0.0	0.0	2.6
Magnesium oxide	0.0	0.0	0.0	0.0	2.0
Sodium bicarbonate	0.0	0.0	0.0	0.0	7.5
Choline chloride	0.0	0.0	0.0	0.0	2.5
Potassium chloride	0.0	0.0	0.0	0.0	2.9
Vitamin–mineral premix2	5.0	5.0	5.0	5.0	5.0
Chromic oxide premix3	25.0	25.0	25.0	25.0	25.0
Total	1,000	1,000	1,000	1,000	1,000

¹Solka-Floc 40 FCC (International Fiber Corporation, Urbana, OH).

²Provided the following quantities per kilogram of complete diet: vitamin A, 8,575 IU; vitamin D₃, 4,300 IU; vitamin E, 28.6 IU; menadione, 7.30 mg; riboflavin, 9.15 mg; _D-pantothenic acid, 18.3 mg; niacin, 73.5 mg; choline chloride, 1,285 mg; vitamin B₁₂, 0.02 mg; biotin, 0.09 mg; thiamine mononitrate, 3.67 mg; folic acid, 1.65 mg; pyridoxine hydrochloride, 5.50 mg; I, 1.85 mg; Mn, 180 mg; Cu, 7.40 mg; Fe, 73.5 mg; Zn, 180 mg; and Se, 0.43 mg.

³Prepared by adding 5 g chromic oxide to 20 g sucrose.

Table 3.

Analyzed concentration of dry matter, CP, and AA in experimental diets, g/kg as-fed basis

	Diet
Item	HFM	FDPP	PM	MBM	NFD
Dry matter	947	950	954	954	963
CP1	168	157	159	149	10.9
Indispensable AA
Arg	10.4	9.4	10.2	9.6	0.0
His	1.2	2.9	2.3	3.0	0.0
Ile	7.8	5.8	4.5	4.1	0.0
Leu	12.7	10.2	8.3	9.3	0.1
Lys	3.7	8.9	7.6	8.0	0.1
Met	1.2	2.8	2.4	1.9	0.1
Phe	7.6	5.8	5.2	5.4	0.1
Thr	7.1	5.6	4.8	4.7	0.0
Trp	0.9	1.4	1.0	1.2	0.0
Val	12.3	7.3	5.9	6.8	0.1
Disposable AA
Ala	7.4	9.7	11.4	11.2	0.1
Asp	10.4	11.8	11.0	11.2	0.1
Cys	8.2	1.9	1.1	1.3	0.0
Glu	16.9	18.7	18.1	17.6	0.1
Gly	12.5	13.7	20.6	19.5	0.1
Pro	15.6	9.0	12.3	12.0	0.2
Ser	14.7	5.5	4.6	5.1	0.1
Tyr	3.6	3.8	3.0	2.9	0.0

¹Analyzed nitrogen concentration multiplied by 6.25.

Experiment 1: Digestibility of CP and AA for broiler chickens

Male broiler chickens (Cobb 500; Cobb-Vantress Inc., Siloam Springs, AR) with a mean body weight (BW) of 43.4 g were obtained from a commercial hatchery at day 0 post hatching. Birds were individually tagged with identification numbers and housed in electrically heated battery brooders (model SB 4 T; Alternative Design Manufacturing, Siloam Springs, AR). The temperature of battery brooders was set at 35 °C on day 0 posthatching and gradually decreased to 27 °C during 22 d of housing. Birds were fed a corn–soybean meal-based standard starter diet containing 210 g CP/kg for 18 d. On day 18 posthatching, birds were individually weighed (mean initial BW = 705 ± 100 g), and 416 birds were assigned in a randomized complete block design with BW as a blocking factor to 5 dietary treatments. Each dietary treatment consisted of 8 replicates with 10 birds per cage for the diets containing test ingredients and with 12 birds per cage for the NFD. Birds had free access to feed and water for 5 d of experimental period. On day 23 posthatching, birds were euthanized by CO₂ asphyxiation, and the ileum (i.e., a portion of the small intestine from the Meckel’s diverticulum to approximately 2 cm proximal to the ileocecal junction) was excised for the collection of ileal digesta from distal two-thirds of the ileum. Ileal digesta samples were pooled within cages and immediately stored at –20 °C.

Experiment 2: Digestibility of CP and AA for pigs

Ten barrows were surgically fitted with T-cannulas at the distal ileum as described by Dilger et al. (2004). After 7 d of recovery period, pigs (mean initial BW = 22.1 ± 1.59 kg) were divided into 2 blocks based on BW and assigned to a duplicate 5 × 4 incomplete Latin Square design with 5 dietary treatments and 4 periods. During the experimental period, pigs were individually housed in metabolism crates (1.22 × 1.22 m) equipped with a feeder and a nipple drinker, and the temperature of experimental facility was maintained between 20 and 25 °C.

Individual BW of pigs was measured at the beginning of each period to calculate the daily feed allowance at 4% of mean BW within blocks, which was divided into 2 equal meals and provided to pigs at 0800 and 1700 hours. Each experimental period consisted of 5 d of adaptation and 2 d of ileal digesta collection. During collection, ileal digesta samples were collected with plastic sample bags (Whirl-Pak bag; NASCO, Fort Atkinson, WI) attached to T-cannulas from 0830 to 1700 hours. Plastic sample bags were prepared to contain 10 mL of 10% formic acid and changed every 30 min. Collected ileal digesta samples were immediately stored at –20 °C. At the end of experiment, frozen ileal digesta samples were slightly thawed and pooled within pigs and diets. Approximately 300 mL was subsampled from pooled and homogenized ileal digesta samples and stored at –20 °C.

Chemical analysis

Ileal digesta samples collected from broiler chickens and pigs were freeze dried before chemical analyses. Test ingredients, experimental diets, and ileal digesta samples were finely ground through 0.75 mm screen using a centrifugal grinder (ZM 200; Retsch GmbH, Haan, Germany). Ground samples were analyzed for dry matter by drying at 105 °C for 24 h in a forced-air drying oven [Precision Scientific Co., Chicago, IL; method 934.01; Association of Official Analytical Chemists (AOAC), 2006]. The concentration of nitrogen in ground samples was analyzed by a combustion method (TruMac N; LECO Corp., St. Joseph, MI; method 990.03; AOAC, 2000), and the concentration CP was calculated as the product of nitrogen concentration and 6.25. Gross energy in test ingredients was analyzed using an isoperibol bomb calorimeter (model 6200; Parr Instrument Co., Moline, IL). Ground samples were analyzed for AA at University of Missouri Agricultural Experiment Station Chemical Laboratories (Columbia, MO). For the preparation of AA analysis, ground samples were hydrolyzed by 6 M HCl (or BaOH for Trp analysis) at 110 °C for 24 h under nitrogen atmosphere. For the analysis of Met and Cys, samples were oxidized by performic acid before acid hydrolysis. The concentration of AA in samples was analyzed by a high-performance liquid chromatography after postcolumn derivatization [method 982.30 E (a, b, c); AOAC, 2006]. Ground samples of test ingredients were analyzed for acid-hydrolyzed ether extract (AEE; method 954.02; AOAC, 2006) and ash (method 942.05; AOAC, 2006). The concentration of Cr in ground experimental diets and ileal digesta samples was measured by spectrophotometry (Spark 10M; Tecan Group Ltd., Männedorf, Switzerland) at 450 nm of absorption after the wet digestion in nitric acid and 70% perchloric acid (Fenton and Fenton, 1979).

Calculations and statistical analysis

The SID (%) of CP and AA in test ingredients and BEL of CP and AA [mg/kg dry matter intake (DMI)] in broiler chickens and pigs were calculated as described by Park et al. (2017).

Data outside of 2.5 times interquartile range were considered outliers before statistical analysis (Hoaglin et al., 1986). Data from experiments 1 and 2 were pooled and considered a 2 × 4 factorial arrangement with the effects of species (broiler chickens or pigs) and four experimental diets (HFM, FDPP, PM, or MBM). Data were analyzed by ANOVA using general linear models (SAS Inst. Inc., Cary, NC). The model included species, experimental diet, interaction between species and experimental diet, and block within species as independent variables. The components of Latin Square design in experiment 2 were rearranged as described by Park et al. (2019) to match the blocking factors in the model. If interactions were observed, least squares means of experimental diets and species were separated by the pairwise comparison with the Tukey’s adjustment. In the absence of interaction, least squares means of significant main effects of experimental diets were separated by the pairwise comparison with the Tukey’s adjustment. Data for the BEL of CP and AA in broiler chickens and pigs were analyzed by two-sample, two-tailed t-test using SAS. Standard error of the difference in mean values between broiler chickens and pigs (µ ₁ − µ ₂) were estimated by either pooled or Satterthwaite test depending on the equality of variance. Experimental unit was cage for experiment 1 and pig for experiment 2. Significance of the model and differences among means were set at P < 0.05.

Results

Animals used in all experiments were in good condition. In experiment 2, data from three pigs fed HFM, FDPP, and NFD were outliers as they were outside 2.5 times interquartile range and thus excluded from dataset in statistical analysis.

The BEL of CP and AA in pigs were greater (P < 0.05) than in broiler chickens (Table 4). The BEL of indispensable AA ranged from 45 mg/kg DMI for Trp to 449 mg/kg DMI for Val in broiler chickens and from 87 mg/kg DMI for Met to 791 mg/kg DMI for Arg in pigs. There were interactions (P < 0.05) between experimental diets and species in the SID of CP, His, Lys, Thr, Trp, Val, and all dispensable AA except Tyr (Table 5). Broiler chickens fed MBM had greater (P < 0.05) SID of CP than those fed HFM or FDPP, whereas pigs fed FDPP had greater (P < 0.05) SID of CP than those fed HFM, which was not different from the values observed in pigs fed PM and MBM. In broiler chickens, the SID of Lys in FDPP was greater (P < 0.05) than in HFM but was lower (P < 0.05) than in MBM, which was not different from PM. In pigs, however, the SID of Lys in FDPP and PM were greater (P < 0.05) than in HFM but were lower (P < 0.05) than in MBM. Broiler chickens fed FDPP and PM had greater (P < 0.05) SID of His, Thr, and Trp than those fed HFM but had lower (P < 0.05) SID values than those fed MBM. There was no difference in the SID of His, Thr, or Trp among pigs fed FDPP, PM, or MBM, all of which were greater (P < 0.05) than the values in pigs fed HFM. The SID of Val in MBM was greater (P < 0.05) than in the other test ingredients for broiler chickens, but there was no difference in the SID of Val among test ingredients for pigs. Pigs had greater (P < 0.05) SID of Ile and Met than broiler chickens. In both broiler chickens and pigs, the SID of Arg and Leu in PM were greater (P < 0.05) than in HFM but were lower (P < 0.05) than in MBM. The SID of Ile was lower (P < 0.05) in FDPP than in the other test ingredients for broiler chickens and pigs. The SID of Met and Phe in PM were greater (P < 0.05) than in HFM but were not different from the values in MBM for broiler chickens and pigs.

Table 4.

Basal ileal endogenous losses (mg/kg DMI) of CP and AA for broiler chickens and pigs^1,2

Item	Broiler chickens	Pigs	SED	P-value
CP, g/kg DMI	8.85	21.98	1.337	<0.001
Indispensable amino acid
Arg	179	791	87.3	<0.001
His	83	195	14.8	<0.001
Ile	212	325	33.9	0.005
Leu	283	585	56.1	<0.001
Lys	197	522	62.2	<0.001
Met	62	87	11.2	0.044
Phe	188	349	35.3	<0.001
Thr	412	623	31.4	<0.001
Trp	45	109	8.2	<0.001
Val	449	626	41.6	<0.001
Dispensable amino acid
Ala	219	647	40.8	<0.001
Asp	432	885	63.1	<0.001
Cys	164	201	13.9	0.021
Glu	505	1,094	90.4	<0.001
Gly	260	1,705	157.7	<0.001
Pro	307	7,237	1,031.6	<0.001
Ser	314	600	28.4	<0.001
Tyr	139	245	24.3	<0.001

¹Each mean represents 8 and 7 observations for broiler chickens and pigs, respectively.

²Mean BW of animals was 675 g and 24.4 kg for broiler chickens and pigs, respectively. Mean DMI was 40.8 and 906 g/d for broiler chickens and pigs, respectively.

Table 5.

Standardized ileal digestibility (%) of CP and AA in HFM, FDPP, PM, and MBM fed to broiler chickens and pigs¹

	Broiler chickens				Pigs					P-value
Item	HFM	FDPP	PM	MBM	HFM	FDPP	PM	MBM	SD	Diet	Species	Diet × species
CP	65.8cd	72.7bc	77.1ab	83.0a	62.1d	72.7bc	70.3bcd	69.9bcd	4.95	<0.001	<0.001	0.007
Indispensable amino acid
Arg	68.8z	77.1y	83.7y	88.5x	69.8z	81.8y	82.8y	85.6x	3.95	<0.001	0.645	0.081
His	55.8d	69.4c	75.6bc	84.2a	60.3d	73.7bc	76.0b	79.6ab	4.05	<0.001	0.286	0.012
Ile	73.7x	69.1y	75.3x	79.4x	77.4x	73.9y	76.8x	78.7x	3.93	<0.001	0.027	0.235
Leu	68.0z	70.8z	77.6y	82.9x	71.9z	75.1z	77.3y	80.5x	3.82	<0.001	0.174	0.057
Lys	55.7d	73.3bc	78.7abc	86.5a	39.0e	70.0c	70.1c	79.2ab	5.35	<0.001	<0.001	0.011
Met	61.4z	75.0y	79.9xy	81.3x	65.6z	78.7y	79.8xy	82.5x	3.63	<0.001	0.021	0.329
Phe	69.6y	71.0y	78.5x	82.7x	73.5y	74.9y	78.1x	80.9x	3.71	<0.001	0.156	0.086
Thr	58.3c	68.4b	74.0b	80.7a	61.1c	70.9b	70.5b	71.7b	4.00	<0.001	0.087	<0.001
Trp	69.5c	82.8b	84.4b	93.3a	61.7c	84.2b	86.5ab	85.9ab	5.05	<0.001	0.030	0.009
Val	69.3c	68.5c	73.9bc	82.8a	72.0bc	72.3bc	73.1bc	76.4ab	4.20	<0.001	0.875	0.007
Dispensable amino acid
Ala	67.2d	75.0c	82.2b	89.0a	65.8d	76.3bc	76.8bc	81.1bc	4.22	<0.001	0.004	0.022
Asp	39.4e	56.2cd	62.2bc	78.2a	38.4e	56.4cd	51.8d	64.4b	4.70	<0.001	<0.001	<0.001
Cys	45.8bc	51.6ab	47.3abc	38.5cd	43.4bcd	56.9a	56.2a	35.9d	5.91	<0.001	0.144	0.019
Glu	59.9c	72.3b	78.2b	84.8a	61.1c	74.8b	73.9b	77.0b	4.04	<0.001	0.050	0.004
Gly	65.2cd	72.3bc	80.8ab	89.7a	61.9d	73.3bc	72.5bc	74.4b	5.66	<0.001	<0.001	0.002
Pro	59.5ab	68.2a	78.3a	87.4a	29.4b	79.2a	89.0a	78.5a	19.69	<0.001	0.403	0.019
Ser	64.3b	66.4b	70.1b	79.2a	65.3b	69.9b	67.4b	68.2b	4.04	<0.001	0.032	<0.001
Tyr	64.5y	72.6x	73.9x	78.7x	65.5y	75.0x	75.2x	75.2x	4.42	<0.001	0.810	0.275

^a–eWithin a row, means with different superscripts differ (P < 0.05).

^x–zWithin a row and species, means with different superscripts differ (P < 0.05).

¹Each least squares mean represents 8 observations except for pigs fed HFM and FDPP (7 observations).

Discussion

Hydrolyzed feather meal mostly consists of feathers from poultry processing, whereas FDPP, PM, and MBM are produced from various inedible portions of carcasses including bone (Hicks and Verbeek, 2016). Therefore, HFM contained greater CP but lower ash concentration compared with the other test ingredients. In addition, because keratin is rich in Cys which mainly forms disulfide bonds (Papadopoulos, 1985), the concentration of Cys in HFM was greater than the other test ingredients. The concentrations of CP and AA in HFM agree with previously reported values (Bandegan et al., 2010; NRC, 2012; Sulabo et al., 2013). In addition, the AEE concentration in HFM is within the range of values reported by Sulabo et al. (2013). Flash dried poultry protein contained greater CP but lower ash concentration than PM, although both FDPP and PM contained similar AEE concentration, probably due to reduced bone contents in order to concentrate the protein contents in FDPP. Published information on the nutrient composition as well as digestibility of nutrients in FDPP is limited, but the concentrations of CP and AA in FDPP were comparable with the values in poultry protein meal (Davies et al., 2019). However, the concentrations of CP and AA in PM were lower than the values reported in previous studies (NRC, 2012; Rojas and Stein, 2013; Yoo et al., 2019). The greater concentration of ash in PM used in the current study compared with previous reports (NRC, 2012; Rojas and Stein, 2013; Yoo et al., 2019) may be due to differences in bone contents which may have affected their CP and AA concentrations. The concentrations of CP and AA in MBM were within the range of previously reported values (NRC, 2012; Adeola et al., 2018; Navarro et al., 2018).

In previous studies conducted to determine the SID of AA for broiler chickens or pigs, experimental diets were formulated to contain CP concentration slightly below the recommended concentration suggested by NRC (1994, 2012). These have generally been approximately 200 g/kg CP for broiler chickens (Adedokun et al., 2007; Kong et al., 2013a; Rochell et al., 2013) and 170 g/kg CP for growing pigs (Dilger et al., 2004; Wang et al., 2018). Therefore, the concentration of CP in experimental diets was set at 160 g/kg in the current study in order to supply CP below the recommendation for both broiler chickens and pigs, although it was quite lower than the recommended concentration of CP in diets for broiler chickens. It was assumed that the SID of CP and AA in test ingredients would be independent to the concentration of CP in experimental diets due to the correction for the BEL of CP and AA (Stein et al., 2007).

Park et al. (2019) reported greater BEL of CP and AA, except for Trp, in pigs than in broiler chickens and discussed that it may be due to the differences in the length of small intestine between broiler chickens and pigs. The results of the current study are consistent with the findings of Park et al. (2019) that pigs had greater BEL of CP and AA compared with broiler chickens, especially for Pro. Adeola et al. (2016) discussed that deficiency of AA by feeding NFD may alter the metabolism of AA in the gastrointestinal tract with potential consequences on BEL of AA, especially for Pro and Gly. Based on the BEL of Pro observed in the current study, it is speculated that the potential impact of AA deficiency on intestinal AA metabolism is greater in pigs than broiler chickens possibly due to the greater capacity and longer gastrointestinal tract of pigs. The BEL of CP and AA in pigs agree with the mean values summarized in previous reports (NRC, 2012; Park et al., 2013; Adeola et al., 2016) except for Arg at 791 mg/kg DMI, which was greater than the mean values but is close to the values reported in other studies (Rojas and Stein, 2013; Sulabo et al., 2013; Navarro et al., 2018). The BEL of CP and AA in broiler chickens are close to the values reported by Park et al. (2019); however, those were lower than the values reported in other studies (Kong and Adeola, 2013a, b; Park et al., 2017; Osho et al., 2019), especially for the BEL of Arg, Leu, Lys, and Phe. This discrepancy may be due to the differences in experimental conditions or procedures among studies. One of the major differences among studies is the ingredient composition of NFD. Nitrogen-free diet used in the current study and Park et al. (2019) were prepared based on sucrose and cornstarch, whereas NFD in the other studies were prepared based on dextrose and cornstarch (Kong and Adeola, 2013a, b; Park et al., 2017; Osho et al., 2019). Kong and Adeola (2013c) reported that broiler chickens fed NFD containing dextrose without cornstarch had greater BEL of CP and most AA than those fed NFD containing dextrose and cornstarch or cornstarch without dextrose. Therefore, the source of carbohydrates in NFD may affect the BEL of CP and AA in broiler chickens. In addition, Cobb 500 broiler chickens were used in both Park et al. (2019) and the current study, whereas Ross 708 (Kong and Adeola, 2013a, b; Park et al., 2017) or Ross 308 (Osho et al., 2019) broiler chickens were used in other studies. Kim and Corzo (2012) reported that the apparent ileal digestibility (AID) of most AA in animal by-product blend were different between the two strains of broiler chickens. Because the AID of AA was not corrected for the BEL of AA, it may be speculated that the BEL of AA is affected by strains of broiler chickens, leading to the different AID of AA in the same feed ingredient. Further research is needed to verify the differences in BEL of AA as well as digestibility of AA among strains of broiler chickens.

Both experiments 1 and 2 were conducted according to the general procedures which have been widely used to determine the AA digestibility in broiler chickens and pigs, respectively (Kong and Adeola, 2014). Consequently, there were several differences in practices between experiments 1 and 2 such as feeding (ad libitum in broiler chickens vs. restricted feeding in pigs) or collection of ileal digesta samples (euthanizing in broiler chickens vs. using T-cannulas in pigs), all of which may affect the results of the current study. However, procedures have been developed to minimize the potential errors, which vary among species of animals. Therefore, despite the differences in practices, recommended procedures for each species were used in the current study for representative results in each experiment.

Pigs had greater SID of Ile and Met than broiler chickens, which is consistent with Park et al. (2017) which reported that the SID of most AA in full-fat soybean, soybean meal, and peanut flour for pigs were greater than the values for broiler chickens. On the other hand, interactions between experimental diets and species were observed in the SID of CP, His, Lys, Thr, Trp, Val, and all dispensable AA except Tyr. This finding is similar with the results observed by Park et al. (2019) in which there were interactions in the SID of most AA between experimental diets containing canola products and species of non-ruminant animals. In the current study, interactions were mainly observed because the SID of several AA in FDPP and PM were lower than in MBM for broiler chickens, but not for pigs. The reason for this difference remains unclear. Perhaps heat damage during processing of FDPP and PM reduced the SID of several AA in broiler chickens, whereas in pigs, the extent of heat damage was not critical to reduce the SID of several AA in FDPP and PM relative to MBM. Shirley and Parsons (2000) reported that the true ileal digestibility of AA in MBM determined by precision-fed cecectomized rooster decreased with increasing pressure and temperature during processing of MBM. Bellagamba et al. (2015) also reported that the in vitro protein digestibility of processed poultry protein was reduced by heat processing compared with freeze-drying. However, information for the comparison of critical temperature of meat by-product processing between broiler chickens and pigs is limited. Batterham and Darnell (1986) reported that the availability of Lys in MBM determined by the slope-ratio assay decreased as the cooking temperature increased in both broiler chickens and pigs, but the extent of the reduction in the availability of Lys was similar between broiler chickens and pigs. Park et al. (2017) discussed that pigs may have greater digestibility of AA than broiler chickens due to the slower passage rate of digesta and longer small intestine in pigs compared with broiler chickens. Therefore, the ability of pigs to digest and utilize AA in heat-damaged proteins may be greater than that of broiler chickens. Further research is needed to verify the critical temperature during the processing that reduces digestibility of AA in FDPP and PM fed to broiler chickens and pigs.

In both broiler chickens and pigs, the SID of most AA in HFM were lower than in the other test ingredients. Papadopoulos (1985) discussed that prolonged autoclaving to hydrolyze keratins may denature proteins resistant to endogenous proteolytic enzymes. On the other hand, incomplete hydrolysis of keratin from inadequate heat processing may also reduce the digestibility of AA in HFM. Therefore, reduced SID of most AA in HFM compared with the other test ingredients could be due to the heat damage during hydrolysis or incomplete hydrolysis of keratin in HFM. Due to the difficulties in optimizing the temperature and processing time of HFM to maximize the hydrolysis with minimal heat damage, the digestibility of AA in HFM may vary among sources with different processing conditions (Wang and Parsons, 1997). Nevertheless, the SID of AA in HFM determined in the current study agree with the previously reported values for broiler chickens (Bandegan et al., 2010) and for pigs (Sulabo et al., 2013).

No difference was observed in the SID of CP and most AA between FDPP and PM for both broiler chickens and pigs, even though PM contained greater concentration of ash than FDPP. Similar with the results of the current study, Rojas and Stein (2013) found that the SID of CP and most AA in chicken meal were not different from the values in poultry by-product meal (PBM) for pigs. Johnson et al. (1998) reported that the concentration of ash in PBM did not affect the true ileal digestibility of AA determined by precision-fed cecectomized rooster assay. Therefore, it may be concluded that protein and AA contents derived from poultry by-products have similar digestibility values regardless of the inclusion rate of bone contents. However, it should be noted that the standardized ileal digestible AA contents in PM are lower than the values in FDPP due to the dilution of proteins by increased bone contents.

Hicks and Verbeek (2016) reported that the difference between PM and PBM is the necks, feet, undeveloped eggs, and viscera, which are included in PBM, but not in PM; however, due to the large variation in by-product composition and processing among sources of PM or PBM, differences in nutrient compositions between PM and PBM are not clear. The SID of AA in PM for broiler chickens determined in the current study were within the range of SID of AA in 5 different sources of PBM (Bandegan et al., 2010). However, the SID of most AA in PM for broiler chickens were greater than the values in PBM reported in Kim et al. (2011). Moreover, the SID of most AA in PM for pigs determined in the current study were greater than the values in chicken meal and PBM reported in Rojas and Stein (2013) but were lower than the values in poultry by-product suggested in NRC (2012). This discrepancy may be due to the differences in temperature and pressure during processing of products or in composition of by-products. Hicks and Verbeek (2016) suggested that the quality of meat by-products is dependent on various factors including the proportion, types, and characteristics of starting raw material and processing conditions including pressure of steam and temperature during agitation and drying.

Unlike the other test ingredients which exclusively contain by-products from poultry meat production, MBM is produced by rendering of by-products originating from general meat production including beef, pork, and poultry (Hick and Verbeek, 2016). Therefore, MBM may be more susceptible to variation in digestibility of nutrients. Nevertheless, the SID of most AA in MBM are within the range of previously reported values for broiler chickens (Adedokun et al., 2007; Rochell et al., 2013; Adedokun et al., 2014) and for pigs (NRC, 2012; Navarro et al., 2018; Wang et al., 2018). However, it should be noted that previous studies conducted to determine the SID of AA in MBM outnumber studies conducted to determine the SID of AA in poultry by-products, which provide a wider range of SID values in MBM than poultry by-products.

In conclusion, there were interactions in the SID of CP, His, Lys, Thr, Trp, Val, and all dispensable AA except Tyr between meals from rendering and species, most of which were due to the lower SID values in FDPP and PM than MBM for broiler chickens. Pigs had greater SID of Ile and Met in HFM, FDPP, PM, and MBM than broiler chickens. In both broiler chickens and pigs, the SID of most AA in HFM were lower than in the other test ingredients, and those in FDPP were not different from the values in PM.

Glossary

Abbreviations

AA

amino acid

AEE

acid-hydrolyzed ether extract

AID

apparent ileal digestibility

AOAC

Association of Official Analytical Chemists

BEL

basal ileal endogenous losses

BW

body weight

CP

crude protein

DMI

dry matter intake

FDPP

flash dried poultry protein

HFM

hydrolyzed feather meal

MBM

meat and bone meal

NFD

nitrogen-free diet

NRC

National Research Council

PBM

poultry by-product meal

PM

poultry meal

SID

standardized ileal digestibility

Acknowledgments

The authors are grateful to Dr. Randy T. Ray (Darling Ingredients Inc., Cold Spring, KY) for facilitating the procurement of poultry by-products and meat and bone meal. The authors acknowledge Dr. Darryl Ragland, Mike L. Zeltwanger, and Patricia A. Jaynes (Purdue University, West Lafayette, IN) for their considerable contribution to this study.

Conflict of interest statement

The authors declare no real or perceived conflicts of interest.