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Animal, page 1 of 7 © The Animal Consortium 2019 animal

doi:10.1017/S1751731119001587

Modeling nutritional and performance factors that influence


the efficiency of weight gain in relation to excreted nitrogen
in weaning piglets
K. M. Cardinal1† , M. S. Vieira1, M. B. Warpechowski2, P. K. Zielgelmann3, L. Montagne4,
I. Andretta1 and A. M. L. Ribeiro1
1
Department of Animal Science, Federal University of Rio Grande do Sul, Porto Alegre, RS 91540-000, Brazil; 2Department of Animal Science, Federal University of Paraná,
Curitiba, PR 80035-050, Brazil; 3Department of Statistic, Federal University of Rio Grande do Sul, Porto Alegre, RS 91509-000, Brazil; 4INRA/AgrocampusOuest, UMR
1079, Systèmes d’Elevage, Nutrition Et Humaine, F. 35000 Rennes, França

(Received 6 August 2018; Accepted 18 June 2019)

One of the most debated topics in pig production is the need to study, understand and change the production system in order to
improve nutrient efficiency, becoming more environmentally friendly. The nitrogen excretion has highly deleterious effects on the
environment, and it is necessary to develop tools that help to reduce the excretion of this compound without compromising
productivity. Therefore, two models were generated to estimate the efficiency of weight gain in relation to excreted nitrogen in
post-weaning piglets. Data for testing these models were obtained from previous master and PhD studies carried out at the
Federal University of Rio Grande do Sul, Animal Science Laboratory using piglets in the post-weaning phase with results for
performance and digestibility. The database that was constructed was composed of raw data from 10 studies carried out
between 2000 and 2016, on a total of 726 piglets weaned at ages between 17 and 28 days, and to which 62 different
treatments were applied. An exploratory analysis of the data was done by evaluating scatter plots and histograms, and variables
representing different treatments were used in a stepwise multiple linear regression analysis, with the F-test used as the selection
criterion. Two models were generated that either considered the nitrogen retained or not, to estimate the ratio between weight
gain and excreted nitrogen using generalized linear model procedure. The authors analyzed the behavior of each variable to
evaluate whether the equation generated was biologically coherent. Weight gain, dry matter intake, nitrogen intake,
metabolizable energy intake, retained nitrogen and urinary nitrogen were all significant ( P<0.001) variables in model I, and in
model II the variable fecal nitrogen was also included. The models had high coefficients of determination ( R2 of model I and II
were 0.9013 and 0.8271, respectively), and the nitrogen ingested variable was the one that most strongly influenced growth
efficiency. When the retained nitrogen variable was removed from the model, there was a reduction in the fit of the equations. It
was possible to conclude that both of the two models generated could be applied and the amount of nitrogen ingested had the
greatest influence on growth efficiency related to nitrogen excretion.

Keywords: meta-analysis, nutrition, protein, pollutant, swine

Implications the modeling carried out in this study will help to reduce nitro-
gen excretion associated with maintenance of weight gain.
The use of easy-to-apply equations to predict the efficiency of
weight gain to excreted nitrogen in weaning piglets has great
relevance within the context of modern, sustainable pig farms.
The equations generated in this study will serve as a supple- Introduction
mentary tool for digestibility assays in research institutions. It
will indirectly benefit pig producers and the environment since Maximizing the growth performance of pigs has traditionally
been the goal of pig producers and nutritionists. Diets are
generally formulated to achieve this goal, and the diets

Present address: Faculdade de Agronomia, Avenida Bento Gonçalves, 7712 – using excessive nutrients result in a surplus of nutrients
Agronomia, RS 91540-000, Brazil. E-mail: katia.zootecnia@hotmail.com excreted in feces and urine (NRC, 2012; Pomar et al.,

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Cardinal, Vieira, Warpechowski, Zielgelmann, Montagne, Andretta and Ribeiro

2017). Consequently, there is an excessive environmental the post-weaning phase (up to 30 days after weaning);
impact caused by the imbalance between the supply of (iii) presented performance results; and (iv) presented
nutrients and the nutritional need of the pigs (Monteiro digestibility results. The first criterion was established to
et al., 2016; Andretta et al., 2017). allow a database of raw data collected under comparable
One of the main nutrients that have negative impacts on conditions. After the selection step, detailed information
the environment is nitrogen (N). During the storage, about the studies was included in the database, including
treatment, and release of waste in the soil, nitrogen can form bibliographic aspects (trial and year), experimental char-
polluting compounds, such as nitrate, ammonia and nitrous acteristics (ingredients and nutritional composition of
oxide (McAuliffe et al., 2016). Laws and regulations to limit diets, sex, age of animals and duration of the trial) and
the production and use of manure as fertilizer have thus results (body weight, weight gain, feed intake, feed con-
become increasingly restrictive, in an attempt to mitigate version, energy, fat, protein and dry matter digestibility
these environmental impacts of N. coefficients, CP, lysine, energy, calcium and phosphorus
In post-weaning piglets in particular, low feed intake intake, urinary nitrogen, fecal nitrogen (FN) and retained
associated with high potential protein deposition results in nitrogen (RN)). In each column a descriptive characteristic
the use of diets with high CP levels. There have been numer- or result was inserted, and in each line the characteristics
ous studies on topics that may result in reduced nutrient and results of an experimental unit (cage with one pig in
excretion, such as on dietary protein reduction using seven studies or mean of two pigs in three studies) were
synthetic amino acid supplementation (Berrocoso et al., described, totaling 144 columns and 491 rows. Some var-
2013; Gloaguen et al., 2013 and 2014), use of exogenous iables were calculated from tabulated data to increase the
enzymes (Guggenbuhl et al., 2012; Metzler-Zebeli and total number of variables, such as lysine intake, feed con-
Zebeli, 2013; Yáñez et al., 2013) and improvements in man- version and the relationship between weight gain and
agement strategies (Hutchings et al., 2013; Montes et al., excreted nitrogen, which was considered as the main
2013; Garcia-Launay et al., 2014). However, high safety mar- response variable in this study. The methodologies
gins are still widely used in conventional feeding programs. described in the literature were used for the elaboration
The genetic advances obtained in pig farms were aimed at of the database and for the coding of the data (Sauvant
obtaining animals with higher lean tissue gain and reduced et al., 2005; Lovatto et al., 2007). Codes were used as
maintenance requirements (Boddicker et al., 2011), lower moderating variables in the analysis to account for vari-
heat production (Barea et al., 2010) and better use of ability among the compiled trials (e.g., effect of study).
nutrients. Since growth rate and feed intake are related to The database was built from the responses observed in 10
the productive efficiency, more efficient animals will conse- studies carried out between 2000 and 2016. The database
quently be less polluting. The analysis of six genetic lines of was composed of data for a total of 726 animals (218 females
pigs showed that from 1969 to 2004 there was a 19% and 508 barrows), and the sum of the treatments of the indi-
improvement in N retention, resulting in 20% less excretion vidual studies results in 62. All piglets came from commercial
(Knap and Bishop, 2000). Similarly, Shirali et al. (2012) and genetic lines and were weaned between 17 and 28 days of
Morel and Wood (2005) showed that N excretion was lower age. The piglets’ average ± SD body weight at the beginning
in lean pigs or in pigs with a greater tendency for meat of the pre-starter phases (1 to 14 days post-weaning) was
deposition. 5.05 ± 2.90 kg and 13.38 ± 4.50 kg at the end of the starter
Meta-analysis is a useful tool for grouping data and phase (15 to 28 days post-weaning). They were individually
quantifying results from studies where the focus of the housed in metabolic cages and kept in thermal comfort
research on a particular topic was only secondary, or even during the experimental periods.
nonexistent (Sauvant et al., 2008). Therefore, it is possible The main ingredients used in the diets, their average com-
to make new inferences on a distinct topic based on a data- positions and other descriptive statistics related to the feeds
base of information from previous studies. Thus, the aim of used are presented in Table 1. The diets were formulated with
the present study was to generate predictive equations to nutritional levels recommended by Rostagno et al. (2011) or
estimate the efficiency of weight gain v. excreted nitrogen NRC (2012) and provided ad libitum. Corn and soybean meal
in post-weaning piglets and investigate the influence of were the main sources of energy and protein used in 60%
different variables on this relation. and 98% of the diets, respectively.
An exploratory analysis of the data was done by evaluat-
ing scatter plots and histograms. Correlation analyses were
performed to pre-select the covariate to be used (Table 2;
Material and methods
r<0.700), and to avoid those that would result in multicolli-
A database was constructed in an electronic spreadsheet nearity within the same model. The pre-selected variables
using data from previous studies selected on the basis of were then used in a stepwise multiple linear regression analy-
the following criteria. To be included, studies must have: sis, with the F-test used as the selection criterion. Significant
(i) been carried out at the Federal University of Rio Grande variables were selected to remain in the regression equa-
do Sul (UFRGS) Animal Science Laboratory, basis of tions, while non-significant variables were sequentially
published theses and dissertations; (ii) used piglets in removed; inflation variance factors were also recorded. A

2
Modeling weight gain/excreted nitrogen in piglets

Table 1 Descriptive statistics of the main ingredients and average Table 2 Pre-selected* variables used in a stepwise multiple linear
composition of the piglets’ diets regression analysis to compose models I and II to predict the weight
gain relative to excreted nitrogen (BWG/EN) of piglets
n Mean SD Min Max
All variables Pre-selected
Ingredient (%)
Corn 337 35.14 16.69 0.00 53.30 Soybean meal
Boiled corn 212 38.10 21.94 0.00 62.61 Corn
Soybean meal 481 17.02 9.01 0.00 35.94 Crude protein
Desativated soy 53 8.21 11.61 0.00 30.00 Lysine
Micronizated soy 116 11.55 11.29 0.00 30.00 Methionine
Isolated soy protein 93 2.17 1.95 0.00 5.00 Tryptophan
Whole milk powder 155 6.42 4.94 0.00 15.87 Threonine
Lactose 92 7.27 2.52 0.00 10.00 Metabolizable energy
Glycerol 31 7.58 5.14 0.00 15.00 Metabolizable energy intake X
Corn gluten 399 3.81 1.66 2.00 7.00 Crude protein: Metabolizable energy
Sugar 491 2.99 0.05 2.55 3.00 Dry matter intake X
Swine blood plasma 303 3.19 1.33 1.00 5.00 Nitrogen intake X
Milk serum 336 12.97 4.99 3.63 20.00 Lysine intake X
Nuklospray E501 63 25.08 5.04 20.00 30.00 Methionine intake
Yeast extract 30 2.53 1.81 0.00 5.00 Inicial live weight X
Beta-glucano2 30 0.02 0.01 0.00 0.04 Final live weight
Promosoy 903 61 5.31 1.97 3.32 7.24 Weight gain X
Raw wheat 58 7.89 17.44 0.00 45.76 Feed consumption X
Boiled wheat 58 7.89 17.44 0.00 45.76 Feed conversion ratio
Raw rice 58 7.87 17.38 0.00 45.62 Fecal nitrogen X
Boiled rice 58 7.87 17.38 0.00 45.62 Urinary nitrogen X
Skimmed milk powder 58 12.00 0.00 12.00 12.00 Retained nitrogen Fixed1
Barley 39 10.00 0.00 10.00 10.00
*The variables were pre-selected after correlation analysis (r<0.700).
Oil 246 2.93 1.11 0.73 5.50 1
Fixed: Variable was fixed by the authors to compose the model I and not
Integral rice meal 63 6.97 4.96 0.00 15.00 compose the model II.
Fat 119 3.43 1.65 1.28 5.40
Phosphate 491 1.33 0.27 0.98 1.92
L-Lysine 491 0.43 0.08 0.29 0.57 each variable to evaluate whether the equation generated
DL-Methionine 491 0.22 0.06 0.10 0.35 was biologically coherent and sensible. Descriptive statistics
L-Threonine 430 0.15 0.03 0.06 0.23 (means, deviations and ranges) were calculated for each
L-Tryptophan 311 0.03 0.03 0.00 0.10 selected variable. After generating the first model, the pro-
Acidifying 491 0.27 0.11 0.00 0.40 cedure was performed again, but with the ‘nitrogen reten-
Zinc oxide 491 0.12 0.12 0.00 0.40 tion’ variable removed from the model. Each individual
Antibiotic 491 0.04 0.03 0.00 0.10
animal represented the experimental unit in all studies,
Calculated composition
ME4 (MJ/kg) 491 14.85 7.69 13.36 16.87
and the code for study effect was considered as a random
CP5 (%) 491 20.17 1.32 17.50 24.00 effect into the model. Graphs for predicted and observed val-
Total lysin (%) 491 1.44 0.11 1.13 1.71 ues were generated for each equation using the values of the
Ca6 (%) 491 0.73 0.07 0.60 0.93 trials selected to compose the database. All analyses were
P7 (%) 491 0.48 0.02 0.43 0.55 performed in the statistical software Minitab 18 (Minitab
Fat (%) 391 6.51 2.94 1.17 11.15 Inc., State College, PA, USA), and the variables were consid-
n=Number of rows of database with the ingredient; SD=standard deviation;
ered to have significant effects when P<0.05.
Min=minimum; Max=maximum.
1
Nuklospray E50®(Sloten do Brasil Ltda, Santos, São Paulo, Brasil).
2
Betaglucano (Betamune, Biorigin – São Paulo, Brasil).
3
Promosoy 90® (Central Soya Inc., Chicago, Ill). Results
4
Metabolizable energy.
5
Crude protein. The pre-selected variables are described in Table 2. They had
6
Calcium.
7
Phosphorus. values of correlation between 0.014 and 0.690, and the vari-
ables with the highest values were RN and nitrogen intake (NI)
(0.689) followed by NI and body weight gain (BWG) (0.683).
model was generated to estimate the ratio of weight gain to Descriptive statistics for the variables that were significant in
excreted nitrogen (BWG/EN) using a generalized linear the models are presented in Table 3, and the adjusted coefficient
model procedure. The model was evaluated through graphi- values of the explanatory variables are presented in Table 4.
cal inspection and performing a Ryan–Joiner test for normal- Model II did not include the RN variable, but included
ity on the residuals. The authors analyzed the behavior of FN g/day), which was not included in model I. Figure 1 shows

3
Cardinal, Vieira, Warpechowski, Zielgelmann, Montagne, Andretta and Ribeiro

Table 3 Descriptive statistics of the significant explanatory variables selected to compose models I and II to predict the weight gain relative to
excreted nitrogen (BWG/EN) of piglets
Variable Mean SD Min Max Median

Dependent
Body weight gain/excreted nitrogen 90.99 31.01 37.76 185.52 86.98
Covariate
Urinary nitrogen (g/day) 2.75 1.74 0.37 14.32 2.50
Fecal nitrogen (g/day) 2.33 1.63 0.41 9.89 1.98
Retained nitrogen (g/day) 15.10 6.32 2.49 32.75 14.10
Body weight gain (g/day) 406 147 135 918 383
Dry matter intake (g/day) 590 213 191 1155 569
Nitrogen intake (g/day) 20.20 8.31 7.19 45.59 19.17
Metabolizable energy intake (MJ/kg) 9.836 3.787 0.669 20.18 9.30
SD = standard deviation; Min = minimum;Max = maximum.

Table 4 Model parameters of the explanatory variables adjusted for the weight gain relative to excreted nitrogen (BWG/EN) of piglets
Body weight gain/excreted nitrogen
Model I Model II1
Variables Coefficient CSE P-value Coefficient CSE P-value

Intercept −156.56 9.14 <0.001 83.83 2.25 <0.001


Urinary nitrogen (g/day) −1.774 0.67 0.009 −15.813 0.74 <0.001
Fecal nitrogen (g/day) – – – −11.143 0.71 <0.001
Retained nitrogen (g/day) 3.267 0.00 <0.001 – – –
Body weight gain (g/day) 0.178 0.00 <0.001 0.179 0.00 <0.001
Dry matter intake (g/day) 0.025 0.11 0.047 0.020 2.86 0.047
Nitrogen intake (g/day) −4.844 0.24 <0.001 −1.857 0.32 <0.001
Metabolizable energy intake (MJ/kg) 0.007 0.00 <0.001 0.012 0.00 <0.001
R2 90.13 82.71
CSE=Coefficient standard error.
1
The analysis of model II did not include nitrogen retained (RN).

the observed BWG/EN values compared to those predicted by demonstrating greater accuracy for low and medium values
models I and II. of BWG/EN in both equations.
The equation generated for model I was:

BWG=EN ¼ 156 56  1:77 UN þ 3:26 RN þ 0:17 BWG Discussion



þ0:02 DMI  4:84 NI þ 0:007 MEI R2 ¼ 0:9012 The equations generated in this study make it possible to
(1) extend the exploration of data obtained in digestibility stud-
ies. Besides analyzing the efficiency in the use of a nutrient or
While that for model II was: ingredient, it is also possible to analyze the results in order to
increase environmental sustainability.
BWG=EN ¼ 83:83  15:81 UN  11:14 FN þ 0:179 BWG All predictive variables were obtained only from digesti-
 bility studies and, consequently, the number of variables is
þ0:02 DMI  1:85 NI þ 0:01 MEI R2 ¼ 0:8271 limited in the database. For that reason, some variables were
(2) calculated and all variables with r<0.07 were considered as
predictors. This is a feature that allows the models to be
Where BWG/EN is the ratio between body weight gain and applied in the future, since the equations are simple to inter-
excreted nitrogen; UN is urinary nitrogen; FN is fecal nitro- pret and include variables that are often used in digestibility
gen; RN is nitrogen retained; BWG is weight gain; DMI is studies, such as ‘Fecal Nitrogen’, ‘Urinary Nitrogen’ or
dry matter intake; NI is nitrogen intake; and MEI is metabo- ‘Retained Nitrogen’. Another limitation of database was that
lizable energy intake. some variables, as ingredients, were not equally distributed
The graphs for observed and predicted values are shown among experiments, which reduced their potential as
in Figure 1. The values presented linear behavior (P<0.001), predictors.

4
Modeling weight gain/excreted nitrogen in piglets

200 200
R 2:90.13 R 2:82.71

Observed BWG/EN
Observed BWG/EN

150 150

100 100

50 50

0 0
0 50 100 150 200 0 50 100 150 200
Predicted BWG/EN Predicted BWG/EN
Equation I Equation II
Figure 1 (colour online) Comparison between observed values of the weight gain/excreted nitrogen (BWG/EN) of piglets and those predicted using models I
and II.

Previous research demonstrated that nutrition and feed- Future studies should be focused to better understand these
ing practices have a direct influence on the environmental patterns to improve the capacity of the models to predict high
impact generated by pig production chain (Cherubini values of BWG/EN.
et al., 2015; McAuliffe et al., 2016). The effect of increased The ability of weaned piglets to preferentially deposit
N intake on performance variables and nitrogen excretion is protein over fat demonstrates the efficiency of growth perfor-
well documented in the literature. However, the relationships mance and N excretion in these animals. The average nitro-
among these variables have not previously been investigated gen retention rate (retention/intake) observed in the studies
to understand the main factors that affect this relationship. that composed our database was 75%, showing that the effi-
From an economic and environmental point of view, it is ciency of the use of this nutrient was high, and it is in accor-
desirable that BWG is maximized while N excretion is dance with values of nitrogen retention found by Straarup et
minimized (Pomar et al., 2017). al. (2006). In contrast, when pigs were evaluated in the
In general, the means of feed intake and weight gain grower-finishing phase, when they were fed on cereal-based
observed in the database constructed in this study were diets, only 35% of the ingested nitrogen was retained
within the expected range for the evaluated range of piglet (Dourmad et al., 1999 and 2009). Shirali et al. (2012)
weights. The good performance observed was likely related revealed that nitrogen excretion is changing throughout
to the high nutrient digestibility coefficients of the feed used, the entire growing period. Greatest nitrogen retention rate
which reached mean values >80%. This was due to the qual- (32%; nitrogen retention/NI), least nitrogen excretion and
ity of the diets, which were formulated with ingredients of greatest retention were found during early growth from 60
high digestibility and associated with good animal health to 90 kg. Nitrogen efficiency gradually decreased with
status. increasing growth stages.
As expected, model I had a higher coefficient of determi- Energy and protein are the major nutritional factors
nation than model II (R2=0.9013 v. 0.8271), due to the better involved in protein gain efficiency in young piglets. Van
adjustment of predicted values by information on N reten- Milgen and Noblet (2003) reported that the response of pro-
tion. This result is coherent with the importance of the tein gain to energy intake is curvilinear, and protein enhance-
self-explanatory RN variable within model I. Although model ment in growing animals is protein- and energy-dependent.
II presents a lower R2, this model may also be an alternative The relationship between energy and BWG/EN in our results
to be used in studies that measure urinary N and fecal N. The showed that higher metabolic energy intake (MEI) resulted in
relation between predicted and observed BWG/EN is not increased growth efficiency. According to Möhn and De
totally linear (Figure 1). The models fit better for the BWG/ Lange (1998), in a stress-free environment with adequate
EN ranges where there are more observations in the database supplies and intake of energy and nutrients, the amount
for the models to be calibrated, and therefore it is possible to of protein deposition is determined by energy intake or
observe that higher values of BWG/EN make the equations the genetic potential for maximum deposition. Thus, the
less precise. It may be associated with different factors, such main nutritional limitation of protein deposition in young
the ingredients’ digestibility, that decrease along the feeding pigs is energy consumption (Dunshea et al., 1998).
phases, or the age of the pigs, because of the decrease in The strategy of increasing dietary energy concentration has
nitrogen retention efficiency. Also, equation 2 has high vari- been used to minimize the impacts of the lower performance of
ability than equation 1 with higher BWG/EN values. Since the piglets in the initial phase (Beaulieu et al., 2006; Oresanya et al.,
main difference between the equations 1 and 2 is FN and 2008). Ribeiro et al. (2016) and Arnaiz et al. (2009) observed
nitrogen retained, the greater variability indicates that the higher feed intake and N retention when dietary energy content
nitrogen retained can be more accurate that the first one. was increased. In our model equations, increased MEI resulted

5
Cardinal, Vieira, Warpechowski, Zielgelmann, Montagne, Andretta and Ribeiro

in improved growth v. N excretion efficiency. Therefore, the and the amount of nitrogen ingested was the variable that
strategy of increasing the concentration of energy in feed could had the greatest influence on efficiency in both models.
also be used to reduce the environmental impact of raising pigs, When the ‘nitrogen retained’ variable was removed from
since the model shows an increment of the efficiency increasing the model, there was a reduction in the fit of the model
energy intake. equation.
The result of increasing NI, in both equations, was a reduc-
tion in growth efficiency. However, nutritional plans with
high levels of CP are frequently used for weaned piglets Acknowledgements
under practical conditions. For most nutrients ingested, maxi- We thank the Animal Research Laboratory (LEZO) of the
mum retention is achieved on a decreasing efficiency curve, Universidade Federal do Rio Grande do Sul – Brazil for
and this is particularly true for proteins and amino acids; as providing the material and data of the digestibility assays.
ingestion increases, there is an increase in rates of degrada- K. M. Cardinal, 0000-0002-8419-509X
tion and excretion by the animal (Rezaei et al., 2013). High
levels of dietary protein increase amino acid deamination,
with a consequent increase in heat production (Roth et al., Declaration of interest
1999; Van Milgen and Noblet, 2003) and reduction in the We declare no conflict of interest, including financial, personal
energy available for protein deposition (Le Bellego et al., or other relationships with other people or organizations that
2001), making the growth process less efficient in terms of could inappropriately influence this work.
both performance and excretion. Webb et al. (2014) reviewed
studies that evaluated the relationship between reduced CP Ethics statement
in the diet and N excretion and concluded that for each 1 unit This study was performed with data from published theses and
reduction in CP, nitrogen excretion can be reduced by up to dissertations; consequently there was no use of animals. In this
10%. Therefore, considering the high efficiency of weaned situation, it is not necessary for the study to be approved by the
piglets in depositing protein and the high safety margins used Animal Ethics Committee of the Universidade Federal do Rio
in diet formulations, the best strategy to improve efficiency Grande do Sul.
and reduce the amount of N excreted would be to reduce
their intake of this element, and perhaps tolerate lower
growth rates (Yin et al., 2010; Gloaguen et al., 2014). Software and data repository resources
The estimated BWG/EN ratio used in this study can assist None of the data were deposited in an official repository.
in improving the productivity and sustainability of current
swine production methods, and is also easy to interpret. It
should, however, be remembered that a static model is References
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