Services on Demand

Article

pdf in Spanish

Article in xml format

Article references

How to cite this article

Automatic translation

Send this article by e-mail

Indicators

Cited by SciELO

Access statistics

Related links

Share

Share on deliciousShare on googleShare on twitterShare on diggShare on citeulike

ServicesMore

More Sharing


More Sharing ServicesMore

Permalink

Revista Lasallista de Investigacin

Print version ISSN 1794-4449

Rev.LasallistaInvestig.vol.6no.1CaldasJan./June2009

Artculo original

Metodologas utilizadas para la medicin de las prdidas

intestinales de nitrgeno endgeno en cerdos
Methodologies used for the measurement of endogenous
intestinal nitrogen losses in growing pigs
Metodologias utilizadas para a medio das perdas intestinais de
nitrognio endgeno em porcos.
Jos Julin Echeverri Zuluaga*, Andrs Gomz Zapata**, Jaime Eduardo Parra Suescn***

Zootecnista, MsC Biotecnologa Animal, Profesor Auxiliar, Departamento de

Produccin Animal, Facultad de Ciencias Agropecuarias, Universidad Nacional de
Colombia, Sede Medelln.
**
Zootecnista, Aspirante a Maestra en Biotecnologa Animal, Universidad Nacional de
Colombia, Sede Medelln, Facultad de Ciencias.
***
Zootecnista, MsC Nutricin Animal, Profesor Auxiliar, Departamento de Produccin
Animal, Facultad de Ciencias Agropecuarias, Universidad Nacional de Colombia, Sede
Medelln. jeparrasu@unalmed.edu.co
*

Resumen
La digestibilidad ileal de los aminocidos es uno de los factores ms importantes para
determinar el valor nutricional de un alimento. Sin embargo, los valores obtenidos en las
pruebas de digestibilidad ileal pueden variar de acuerdo con las prdidas de nitrgeno
endgeno del animal y por esto, pueden ser expresados como aparentes o verdaderos. En
la determinacin del valor aparente no se tienen en cuenta las prdidas de nitrgeno
endgeno, por lo que se subestima la cantidad de aminocidos absorbidos durante la

digestin. Al tomar en cuenta el componente endgeno, la digestibilidad ileal se transforma

en verdadera, siendo sta el mejor parmetro para representar los aminocidos absorbidos
en el tracto digestivo. Las prdidas de nitrgeno endgeno han sido clsicamente definidas
como el nitrgeno encontrado en la digesta o en las heces de animales alimentados con
dietas libres de nitrgeno. Tradicionalmente, las prdidas de nitrgeno endgeno en cerdos
han sido determinadas mediante los mtodos de regresin lineal o por el de ofrecer dietas
libres de nitrgeno. Actualmente se han desarrollado varias tcnicas alternativas para
estimar las prdidas de nitrgeno endgeno en cerdos que consumen dietas que contienen
niveles variables de protena. Cada una de estas tcnicas posee limitaciones y todas
requieren diferentes suposiciones. Basados en un creciente nmero de resultados obtenidos
con diferentes tcnicas, las prdidas de nitrgeno endgeno parecen estar altamente
afectadas por el mtodo utilizado para su determinacin y por factores como son peso
corporal, consumo de materia seca, y constituyentes de la dieta (factores antinutricionales,
fibra y protena).
Palabras clave: Flujo de nitrgeno endgeno, cerdos en crecimiento, tcnicas de
cuantificacin.

Abstract
Amino acid ileum digestibility is one of the most important factors to determine the
nutritional value of foods. However, the values obtained in ileum digestibility tests can vary
according to the endogenous nitrogen losses in the animal. Thus, ileum digestibility values
can be classified as apparent or true. When determining the apparent value, endogenous
nitrogen losses are not taken into account and the amounts of absorbed amino acid during
digestion are then underestimated. When the endogenous component is taken into account,
digestibility data become true, being the best parameter to represent absorbed amino acid
in the digestive tract. Endogenous nitrogen losses are classically defined as the nitrogen
found in the digesta or in the feces of animals fed with nitrogen-free diets. Traditionally,
endogenous nitrogen losses in pigs have been determined by feeding nitrogen-free diets or
by the lineal regression method. More recently, several alternative techniques have been
developed to evaluate endogenous nitrogen losses in pigs that are fed with diets that
contain variable protein levels. Each of these techniques has some limitations and all
require different assumptions. Based on the increasing number of results recently obtained
with different techniques, endogenous nitrogen losses seem to be highly affected by the
used method and by factors as weight, dry matter consumption, and diet components (anti
nutritional factors, fiber and protein).
Keywords: Endogenous nitrogen flow, growing pigs, quantification techniques.

Resumo
A digestibilidad ileal dos aminocidos um dos fatores mais importantes para determinar o
valor nutricional de um alimento. No entanto, os valores obtidos nas provas de
digestibilidad ileal podem variar de acordo s perdas de nitrog&ecird;nio endgeno do
animal. Devido ao anterior, os valores de digestibilidad ileal podem ser expressados como
aparentes ou verdadeiros. Na determinao do valor aparente no se tm em conta as

perdas de nitrognio endgeno, pelo que se subestima a quantidade de aminocidos

absorvidos durante a digesto. Ao tomar em conta o componente endgeno, a
digestibilidad ileal se transforma em verdadeira, sendo esta o melhor parmetro para
representar os aminocidos absorvidos no tracto digestivo. As perdas de nitrognio
endgeno foram classicamente definidas como o nitrognio encontrado na digesta ou nas
fezes de animais alimentados com dietas livres de nitrognio. Tradicionalmente, as perdas
de nitrognio endgeno em porcos foram determinadas mediante os mtodos de regresso
linear ou pelo de oferecer dietas livres de nitrognio. Atualmente se desenvolveram vrias
tcnicas alternativas para estimar as perdas de nitrognio endgeno em porcos que
consomem dietas que contm nveis variveis de protena. Cada uma destas tcnicas possui
limitaes e todas requerem diferentes suposies. Baseados num crescente nmero de
resultados obtidos com diferentes tcnicas, as perdas de nitrognio endgeno parecem
estar altamente afetadas pelo mtodo utilizado para sua determinao e por fatores como
so peso corporal, consumo de matria seca, e constituintes da dieta (fatores
antinutricionales, fibra e protena).
Palavras chaves: Fluxo de nitrognio endgeno, porcos em crescimento, tcnicas de
quantificao.

Introduccin
El valor nutricional de un ingrediente para animales puede ser determinado por su
contenido de nutrientes disponibles, en especial por su aporte de aminocidos (AA) y
energa1. La digestibilidad ileal de los AA es uno de los factores ms importantes para
calificar la calidad de la dieta y la respuesta productiva de los animales; la cual, desde hace
aos, se ha determinado en animales monogstricos a travs del muestreo del contenido
ileal2. Sin embargo, los valores obtenidos en las pruebas de digestibilidad ileal pueden
variar de acuerdo con las secreciones intestinales de nitrgeno o prdidas de nitrgeno
endgeno (PNE) del animal y por ello los valores pueden ser expresados como aparentes o
verdaderos. En la determinacin del valor aparente no se tienen en cuenta las PNE, por lo
que se subestima la cantidad de AA absorbidos durante la digestin3. Al tomar en cuenta el
componente endgeno, la digestibilidad ileal se transforma en verdadera, siendo sta el
mejor parmetro para representar los AA absorbidos en el tracto digestivo 4. Por lo anterior,
las PNE en cerdos en crecimiento deben ser determinadas y cuantificadas, ya que stas
pueden afectar la disponibilidad de nutrientes y la respuesta productiva en cerdos en
crecimiento.
1. Prdidas de nitrgeno endgeno
Las prdidas de nitrgeno endgeno (PNE), son clsicamente definidas como el nitrgeno
encontrado en la digesta o en las heces de animales alimentados con dietas libres de
nitrgeno. Estos compuestos provienen principalmente de mucoprotenas 5, enzimas
pancreticas e intestinales, saliva, secreciones biliares y gstricas, clulas descamadas de
la mucosa intestinal, albmina srica, pptidos, aminocidos (AA), amidas, aminas,
glucosaminas6-8 y la protena de origen bacteriano9, aunque esta ltima, estrictamente
hablando, no es nitrgeno endgeno. Sin embargo, las PNE representan slo una fraccin
del total de nitrgeno secretado dentro del intestino y su incremento est asociado
principalmente a una mayor tasa de sntesis de protena intestinal, y a una ineficiente tasa
de sntesis proteica corporal. Aunado a lo anterior, estas prdidas, aumentan el
requerimiento de energa y aminocidos en el animal.

2. Mtodos para estimar las prdidas de nitrgeno endgeno en cerdos

Muchos mtodos han sido desarrollados para cuantificar el flujo de nitrgeno endgeno en
cerdos en crecimiento. Estos mtodos implican la utilizacin de dietas libres de nitrgeno,
que contienen fuentes de protenas que se asumen como 100% digestibles, y tcnicas de
regresin matemtica. En los ltimos tiempos, se han desarrollado tcnicas que incluyen el
uso de marcadores y ultrafiltrado de pptidos en el laboratorio. Entre los mtodos ms
utilizados en experimentacin se encuentran:
Dietas libres de nitrgeno: Esta tcnica consiste en alimentar animales con una dieta
libre de nitrgeno, midiendo el flujo de nitrgeno y AA en la digesta colectada en el leon
distal. Se asume que todo el nitrgeno (N) y los AA que aparecen en la digesta son de
origen endgeno. La principal crtica a este mtodo, es su naturaleza antifisiolgica, porque
disminuye el estmulo de la actividad normal del intestino, afecta el metabolismo de la
protena dietaria, reduce la secrecin de compuestos nitrogenados en el lumen intestinal y
subestima la concentracin de PNE en leon4,10. El resultado obtenido es un balance de
protena negativo11 en los animales evaluados, con un efecto poco representativo sobre las
PNE en el leon distal. Adems, la ausencia de protena en el alimento disminuye las
secreciones endgenas y no hay factores que estimulen su produccin o impidan su
reabsorcin por la pared intestinal12, por cuanto afecta la capacidad de absorcin de los AA
en el intestino delgado debido al contenido de protena en la dieta13. El intestino delgado
responde a una ingesta reducida de protena con el incremento de la absorcin intestinal de
AA14. Adicionalmente, los constituyentes de la dieta, como la fibra y factores
antinutricionales, los cuales estn asociados a la protena de la dieta, podran aumentar las
PNE15-18.
Regresin lineal: El mtodo de regresin lineal (RL), consiste en alimentar al animal,
incrementando las cantidades de N en la dieta (a un consumo constante de materia seca) y
estimar las PNE por extrapolacin del flujo ileal de AA a cero N consumido. Esto permite
que las PNE sean determinadas bajo condiciones normales de alimentacin proteica. La
principal suposicin con este mtodo, es que el incremento en el contenido de N de la
digesta ileal se debe a un incremento proporcional en la cantidad de N diettico
indigestible. Se supone adems, que no hay cambios en la calidad de N endgeno
excretado19. La tcnica de regresin es, potencialmente, el mejor estimador de las PNE,
comparado con las dietas libres de nitrgeno20.
Tcnica de Dilusin Isotpica: El mtodo de Dilusin Isotpica (DI), implica la
marcacin del nitrgeno de la dieta con el istopo pesado 15N13,21. Ha sido utilizado para
marcar cualquier tipo de pool de N en el animal22 o en el N diettico23 y permite una
diferenciacin entre el nitrgeno endgeno y el N diettico no digerido. La cantidad de PNE
puede ser subestimada por este mtodo, ya que no tiene en cuenta las clulas de la
mucosa secretadas por va endgena, las cuales son sintetizadas a partir de AA dietticos
marcados en el lumen24. El N suministrado por los AA dietticos puede ser absorbido e
incorporado rpidamente en las protenas corporales, lo cual complica la diferenciacin del
N no digerible y del NE25.
Tcnica de la Homoarginina: Es una tcnica que involucra la transformacin de la lisina
diettica a Homoarginina (HA), a travs de un proceso de guanidacin (una reaccin con
OMetilisourea)26,27. Esta tcnica permite la diferenciacin entre la lisina diettica (convertida
en HA) y la lisina de la protena del intestino y debe cumplir varios requisitos: a) la
guanidacin de la lisina en la protena a ensayar debe ser uniforme o al menos completa; b)
la guanidacin no debe afectar la digestibilidad de la protena; c) la HA no puede ser
hidrolizada a urea o lisina en el intestino delgado; d) la HA debe ser absorbida y
metabolizada como cualquier AA; e) la HA no puede reingresar al tracto digestivo; f) la
presencia de HA en el plasma o intestino, no debe afectar las PNE28. Con este mtodo, la

lisina no es utilizada para la sntesis de protena, por lo que debe ser usado poco tiempo,
para evitar posibles deficiencias de lisina29. Adems, con esta tcnica la digestibilidad
verdadera de los dems AA no es determinada directamente30.
Protenas hidrolizadas enzimticamente: Esta tcnica permite el flujo de NE y de AA en
el intestino delgado, para ser determinados en animales alimentados con dietas que
contienen protenas y AA como nica fuente de N. Los animales son alimentados con una
dieta en la que la nica fuente de N es casena hidrolizada enzimticamente, la cual
contiene aproximadamente 56% de AA libres y 41% de di-tripptidos con pesos
moleculares menores de 5000 Da31. Se asume entonces, que todo el NE est en fracciones
con pesos moleculares mayores a 10000 Da. De esta manera, al separar pesos moleculares
bajos (<5000 Da) y altos (>10000 Da) de compuestos nitrogenados en la digesta ileal, se
puede hacer una identificacin entre cualquier N exgeno no absorbido y cualquier N de
origen endgeno32. La mayor restriccin de esta tcnica, es que no puede ser usada para
estimar la secrecin de NE donde haya una asociacin directa entre la protena y factores
dietticos, los cuales son conocidos por influenciar las secreciones endgenas y las PNE 10.
Este mtodo puede ser aplicado en alimentos que contengan fuentes de protena animal 33.
Comparacin entre tcnicas para determinar prdidas de nitrgeno endgeno: En
la literatura no se han reportado estudios en los que se comparen y evalen todas las
tcnicas para determinar las PNE al mismo tiempo. Sin embargo, muchos estudios han
comparado algunas de estas tcnicas en cerdos (tabla 1), donde se ha observado que las
PNE difieren entre mtodos. El trabajo realizado por Roos et al23, indica que cuando se
utiliza la tcnica de HA se encuentran valores de PNE altos, comparados con los obtenidos
con la tcnica de DI. Esto puede deberse a que con la tcnica de DI el N marcado puede ser
absorbido e incorporado dentro de los diferentes ciclos de protena de reciclaje intestinal, y
por ltimo, puede volver a ser secretado hacia el intestino delgado. Con la tcnica de
protenas hidrolizadas enzimticamente se obtienen mayores valores de PNE, al ser
comparada con las tcnicas de DLN y RL. Al parecer, la tcnica de PHE induce mayores PNE,
confrontadas al ofrecer dietas que se asumen como 100% digestibles. Lo anterior evidencia
que los pptidos suministrados, ya sea como tales o derivados de la digestin natural de las
protenas dietarias, tienen influencia en las PNE del tracto digestivo1, 6. En una comparacin
directa, los resultados obtenidos con la tcnica de PHE fueron similares a los obtenidos con
la tcnica de DI. Los resultados de estos estudios (tabla 1) sugieren que los mtodos
convencionales (DLN, RL y PHE) resultan en una subestimacin de PNE en cerdos
alimentados con dietas que contienen diferentes fuentes y niveles de protenas. Adems,
estos resultados indican que los valores obtenidos de PNE son altamente variables34.

3. Factores que afectan las prdidas de nitrgeno endgeno en cerdos.

Adems de las tcnicas anteriormente mencionadas, existen varios factores que pueden
afectar los resultados y mediciones de las PNE en cerdos en crecimiento. As mismo, la
secrecin y reabsorcin de NE en el tracto gastrointestinal pueden estar influenciadas por
muchos factores, entre los que se pueden encontrar:
Consumo de materia seca (MS) y peso corporal: Aparentemente, el efecto de la
materia seca MS, consumida sobre las PNE est relacionado con el peso corporal del
animal34, 36. Posiblemente, esto se deba a que los animales aumentan su consumo y
comienzan a ser ms pesados; se podra esperar que a mayor consumo de alimento, mayor
es la secrecin de las enzimas digestivas, las cuales contribuyen a aumentar el flujo de AA
endgenos37. Liddle et al.38 han demostrado el efecto positivo que tiene la concentracin de
sustrato en la dieta (protena, carbohidratos, grasas) sobre la secrecin y actividad de
algunas enzimas pancreticas.
Procesamiento del alimento: Los alimentos molidos disminuyen el tamao de la
partcula (aumentando la superficie de contacto), la cual es expuesta a enzimas digestivas,
mejorando la digestibilidad ileal de N y la utilizacin del alimento 39. Los tratamientos
trmicos son procesos que tienen efectos importantes en la digestibilidad ileal de N, ya que
pueden destruir algunos factores antinutricionales contenidos en los alimentos, como las
lectinas, factores inhibidores de proteasas, taninos, etc. Los tratamientos trmicos ms
comnmente utilizados son: La extrusin, cocimiento y torrefaccin40. El descascarillado, es
otro tratamiento mecnico de gran importancia, debido a que disminuye el contenido de
fibra y de taninos de algunas materias primas, localizadas principalmente, en la cscara de
leguminosas.

Factores antinutricionales: Estos han sido reportados para aumentar el flujo de NE en el

leon de cerdos. Los Inhibidores de Tripsina (IT)41, Lectinas42 y Taninos43 elevan la cantidad
de N y NE que pasan al leon terminal. Los taninos disminuyen la digestibilidad de N debido
a que tienen la capacidad de unirse a las protenas de la dieta, mediante la formacin de
puentes de hidrgeno e interacciones hidrofbicas de sus grupos hidrxilos con los grupos
carbonilo de las protenas dietticas, disminuyendo la actividad de la pepsina gstrica, la
tripsina, la quimotripsina pancretica y las peptidasas intestinales del borde en cepillo. Por
otro lado, los taninos actan negativamente al cambiar la morfologa de la mucosa
gastrointestinal, disminuyendo la absorcin transmembranal de nutrientes y al incrementar
las secreciones endgenas de protena44. Los IT interfieren directamente con la digestin
del N de la dieta por unirse en forma irreversible a la tripsina y quimotripsina. Adems, los
IT estimulan la secrecin compensatoria de estas enzimas pancreticas y como resultado,
se da un incremento en las PNE45. Los IT disminuyen la digestibilidad aparente de la
cistena, debido a que cerca del 50% de la cistena en las leguminosas se localiza en los
inhibidores de tripsina. Adems, como las enzimas pancreticas son ricas en este
aminocido, la formacin de complejos irreversibles entre los IT con tripsina y
quimotripsina, incrementan las prdidas endgenas de cisteina45. Las lectinas son protenas
que tienen la capacidad de unirse a azcares especficos, como la matriz de carbohidratos
de la pared intestinal y del borde en cepillo, aumentando las prdidas de NE. Las lectinas
estimulan la proliferacin de bacterias en el lumen, debido a una gran disponibilidad de
nutrientes para las bacterias y una alta tasa de recambio celular, al tiempo que crece el
nmero de sitios potenciales de unin para las bacterias en las clulas epiteliales 42.
Contenido y calidad de la fibra dietaria: Las secreciones de jugos pancreticos, bilis y
moco, se incrementan cuando aumenta el consumo de pectinas y celulosa46. Las pectinas
poseen propiedades de viscosidad y gelificacin que disminuyen la digestin y absorcin de
nutrientes al reducir la mezcla de los contenidos intestinales e interferir con la unin de
enzima-sustrato y formar una capa de agua esttica que crea una barrera fsica para la
absorcin de nutrientes10. Estos componentes pueden interactuar con los AA liberados
durante la hidrlisis de las protenas y permitir que algunos escapen a la absorcin en el
intestino delgado (llegando al leon distal), para luego pasar al intestino grueso 47. Este
componente tambin aumenta la secrecin y prdidas de mucinas e induce la proliferacin
de las clulas epiteliales y mucosas.
Fuentes y solubilidad de la protena: Las fuentes de protena animal son ms
digestibles que las fuentes de protena vegetal, por cuanto los cambios en la composicin
de las protenas de las plantas pueden causar cambios en la digestibilidad ileal de AA en
cerdos48. Aunado a esto, la presencia de factores antinutricionales en alimentos vegetales
puede disminuir la digestibilidad de los AA. La solubilidad de una protena en un medio
acuoso, como es el tracto gastrointestinal, es un factor determinante en la digestibilidad
ileal aparente de AA, ya que propicia un medio nico para la fcil unin entre enzimasustrato49.
Cantidad y fuente de grasa diettica: La cantidad de grasa en la dieta afecta la
digestin de protenas en cerdos. En estudios con cerdos en crecimiento, se present un
efecto lineal significativo a medida que aument la ingesta de grasa en la dieta. La grasa
dietaria disminuye el tiempo de trnsito en el intestino delgado, lo cual permite un mayor
tiempo de digestin y absorcin de los AA antes de llegar al leon terminal40. Un incremento
en la grasa de la dieta retrasa el vaciado gstrico, lo que podra resultar en unabaja tasa de
pasaje de la dieta en el intestino delgado, a su vez, en una alta tasa de digestibilidad de los
AA. Esto es particularmente cierto, cuando el tiempo requerido para la digestin de las
protenas y la absorcin de los AA es un factor limitante50.

Conclusiones
Esta revisin ha sido desarrollada con el fin de demostrar la importancia de las PNE en el
leon distal, y su efecto sobre la nutricin de cerdos en crecimiento. Muchos estudios
citados en esta revisin se centran en las metodologas, para estimar las PNE, y en los
efectos de los componentes dietarios sobre las PNE. El mtodo utilizado para determinar las
PNE tiene gran influencia sobre la cuantificacin del flujo de nitrgeno en ingredientes
utilizados en nutricin animal. Los mtodos convencionales (DLN, RL y PHE) subestiman las
PNE en cerdos alimentados con dietas que contienen diferentes fuentes y niveles de
protena. Estos estudios sugieren que la tcnica de la Homoarginina (HA) podra ser una
buena opcin para la determinacin de las PNE en una gran cantidad de alimentos. Basados
en los resultados obtenidos con estas tcnicas, las PNE parecen estar altamente afectadas
por factores como el peso corporal, consumo de materia seca, fibra, contenido de factores
antinutricionales y protena (digestible) en la dieta. Una reduccin en las PNE puede
mejorar la eficiencia de la utilizacin de los aminocidos y energa de la dieta en la
produccin de cerdos. Por tanto, los componentes especficos que causan estas prdidas en
dietas e ingredientes alimenticios para cerdos deben ser identificados.

Referencias
1. GUTIRREZ C., Lourdes, et al. Comparacin de mtodos para determinar el flujo ileal de
aminocidos endgenos y la digestibilidad verdadera de aminocidos de harina de pescado
suministrada a ratas. En: Revista Cientfica. Septiembre-octubre, 2005, vol.15, no.5, p.451457.
[ Links ]
2. JORGENSEN, H.; SAUER, W.C. and THACKER, P.A. Amino acid availabilities in soybean
meal, sunflower meal, fish meal and meat and bone meal fed to growing pigs. En: Journal
of Animal Science. March, 1984. vol. 58, no 4, p.596-604.
[ Links ]
3. ARENTSON, R.A. and ZIMMERMAN, D.R. True digestibilities of amino acids and protein in
pigs using C13 as a label to determine metabolic amino acid excretion. En: Journal of Animal
Science. 1992. vol. 70, Suppl. 1, p.68.
[ Links ]
4. DARRAGH, A.J.; MOUGHAN, P.J. and SMITH, W.C. The effect of amino acid and peptide
alimentation on the determination of endogenous amino acid flow at the terminal ileum of
the rat. En: Journal of the science of food and agriculture. 1990. vol. 51, no. 1, p.4756.
[ Links ]
5. CORRING, T. and JUNG, J. The amino acid composition of pig pancreatic juice. En:
Nutrition Reports International. 1972. vol. 6, p.187-198.
[ Links ]
6. SOUFFRANT, W.B. Endogenous nitrogen losses during digestion in pigs. En: International
Symposium on Digestive Physiology in Pigs (5: 24-26, april: Pudoc, Wageningen, The
Netherlands). Memorys. PUDOC, Wageningen Doorwerth, The Netherlands: Verstegen.
M.W.A; Huisman, J.and den Hartog, L.A, 1991. p. 147-166.
[ Links ]
7. MOUGHAN, Paul J., et al. Evaluation of the isotope dilution technique for determining ileal
endogenous nitrogen excretion in the rat. En: Journal of the Science of Food and
Agriculture. 1992. vol. 58, no. 2, p. 165-172.
[ Links ]

8. JANSMAN, A. J., et al. Evaluation through literature data of the amount and amino acid
composition of basal endogenous crude protein at the terminal ileum of pigs. En: Animal
Feed Science and Technology. 2002. vol. 98, no. 1-2, p.49-60.
[ Links ]
9. CAINE, W.R., et al. Apparent ileal digestibilities of amino acids in newly weaned pigs fed
diets with protease-treated soybean meal. En: Journal of Animal Science. 1997. vol. 75, no.
11p.2962-2969.
[ Links ]
10. NYACHOTI, C.M., et al. Significance of endogenous gut nitrogen losses in the nutrition
of growing pigs: A review. En: Canadian Journal of Animal Science. March, 1997. vol. 77,
no. 1, p.149-163.
[ Links ]
11. OTTO, E.R., et al. Nitrogen balance and ileal amino acid digestibility in growing pigs fed
diets reduced in protein concentration. En: Journal of animal Science. July, 2003. vol. 81,
no. 7, p.1743-1753.
[ Links ]
12. LETERME, Pascal, et al. Effect of oral and parenteral N nutrition vs N-free nutrition on
the endogenous amino acid flow at the ileum of the pig. En: Journal of the Science of Food
and Agriculture. 1996. vol. 71, no. 2, p. 265-272.
[ Links ]
13. De LANGE, C.F.M. et al. The effect of protein status of the pig on the recovery and
amino acid composition of endogenous protein in digesta collected from the distal ileum.
En: Journal of Animal Science. 1989. vol. 67, p.755-762.
[ Links ]
14. CHRISTENSEN, H.N. The regulation of amino acid and sugar absorption by diet. En:
Nutrition Reviews. July. 1984, vol. 42, no. 7, p.237-242.
[ Links ]
15. SKILTON, Grant A.; MOUGHAN, Paul J. and SMITH, William C. Determination of
endogenous amino acids flow at terminal ileum of the rat. En: Journal of the Science of
Food and Agriculture. 1988. vol. 44, no. 3, p. 227-235.
[ Links ]
16. MARISCAL, G.; REIS, T.C. e PARRA, J.E. Estimao dos coeficientes de digestibilidade
ileal aparente das protenas e aminocidos da torta de canola em leites recmdesmamados. En: Revista Colombiana de Ciencias Pecuarias. 2008. vol. 21, no. 2, p.201209.
[ Links ]
17. NYACHOTI, C.M.; ATKINSON, J.L. and Leeson S. Sorghum tannins: a review. En:
World's Poultry Science Journal. 1997. vol. 53, p.5-21.
[ Links ]
18. REIS, T.C.; MARISCAL, G. y AGUILERA, A. Efecto de diferentes cereales en dietas de
iniciacin para lechones sobre la digestibilidad sobre la digestibilidad de los nutrimentos y la
referencia alimentaria: En: Veterinaria. Mxico. Enero-marzo, 2005. vol. 36, no. 1, p.1124.
[ Links ]
19. HOOGKINSON, S.M., et al. Effect peptide concentration on endogenous ileal amino
acids loss in the growing pig. En: British Journal of Nutrition. 2000. vol. 83, no. 4, p.421430.
[ Links ]
20. FAN, M.Z.; SAUER, W.C. and MCBURNEY, M.I. Estimation by regression analysis of
endogenous amino acids levels in digesta collected from the distal ileum of pigs. En:
Journal of Animal Science. 1995. vol. 73, no. 8, p.2319-2328.
[ Links ]

21. KRAWIELITZKI, K., et al. Estimation of N absorption, secretion, and reabsorption in

different intestinal sections of growing pigs using the 15N isotope dilution method. En:
International Symposium on Digestive Physiology in Pigs (6: 4-6 october: Bad Doberan,
Danmar). Memorys. Bad Doberan, Danmar: W,B. Souffrant and H. Hagemeister, Proc, 1994.
p.79-82.
[ Links ]
22. SCHULZE, H., et al. Effect of level of dietary neutral detergent fiber on ileal apparent
digestibility and ileal nitrogen losses in pigs. En: Journal of Animal Science. 1994. vol. 72,
no. 9, p.2362-2368.
[ Links ]
23. ROOS, Nils; PFEUFFER, Mara and HAGEMEISTER, Hans. Labelling with 15N as compared
with homoarginine suggest a lower prececal digestibility of casein in pigs. En: Journal of
Nutrition. December, 1994. vol. 124, no. 12, p.2404-2409.
[ Links ]
24. DE LANGE, C.M.M., et al. 15N-Leucine 15NIsoleucine isotope dilution techniques versus
the 15N-Isotope dilution technique for determining the recovery of endogenous protein and
amino acids in digesta collected from the distal ileum in pigs. En: Journal of Animal Science.
1992. vol. 70, no. 6, p.1848-1858.
[ Links ]
25. TAMMINGA, S., et al. The nutritional significance of endogenous N-losses along the
gastrointestinal tract of farms animals. En: Archives of Animal Nutrition. 1992. vol. 48, no,
1-2, p.9-22.
[ Links ]
26. HAGEMEISTER, H. and ERBERSDOBLER, H. Chemical labelling of dietary protein by
transformation of lysine to homoarginine: a new technique to follow intestinal digestion and
absorption. En: The Proceedings of the Nutrition Society. 1985. vol. 44 p.133.
[ Links ]
27. HODGKINSON, S.M.; SOUFFRANT, W.B. and MOUGHAN, P.J. Comparison of the
enzymehydrolyzed casein, guanidination, and isotope dilution methods for determining ileal
endogenous protein flow in the growing rat and pig. En: Journal of Animal Science. 2003.
vol. 81, no. 10, p.2525-2534.
[ Links ]
28. DRESCHER, H., et al. Guanidination (homoarginine- labelling) of proteins does affect
prececal 15N recovery in pigs. En: International Symposium on Digestive Physiology in Pigs
(6: 4-6 october: Bad Doberan, Danmar). Memorys. Bad Doberan, Danmar: W,B. Souffrant
and H. Hagemeister, Proc, 1994. p.64-66.
[ Links ]
29. TEWS, Jean K. and HARPER, Alfred E. Induction in rats of lysine imbalance by dietary
homoarginine. En: Journal of Nutrition. 1986, vol. 116, no. 10, p.1910-1921.
[ Links ]
30. MARTY, B.J.; CHAVEZ, E.R. and DE LANGE C.F.M. Recovery of amino acids at the distal
ileum for determining apparent and true amino acid digestibilities in growing pigs fed
various heatprocessed full-fat soybean bean products. En: Journal of Animal Science. 1994.
vol. 72, p.2029-2037.
[ Links ]
31. LETERME, P., et al. Effect of oral and parenteral N nutrition vs N-free nutrition on the
endogenous amino acid flows at ileum of the pig. En: International Symposium on Digestive
Physiology in Pigs (6: 4-6 october: Bad Doberan, Danmar). Memorys. Bad Doberan,
Danmar: W,B. Souffrant and H. Hagemeister, Proc, 1994. p.60-63.
[ Links ]
32. MOUGHAN, Paul J. and RUTHERFURD, Shane M. Endogenous flow of total lysine and
other amino acids at the distal ileum of the protein- or peptide-fed rat: The chemical

labeling of gelatin protein by transformation of lysine to homoarginine. En: Journal of the

Science of Food and Agriculture. 1990. vol. 52, p.179-192.
[ Links ]
33. DONKOH, A.; MOUGHAN, P.J. and MORE, P.C.H. Comparison of methods to determine
the endogenous amino acids flow at terminal ileum of growing rats. En: Journal of the
Science of Food and Agriculture. 1995. vol. 67, no. 3, p.359-366.
[ Links ]
34. MARISCAL-LANDIN, Gerardo, et al. Endogenous amino nitrogen collected from pigs with
end-toend ileorectal anastomosis is affected by the method of estimation and altered by
dietary fiber. En: Journal of Nutrition. 1995. vol. 125, no. 1, p.136-146.
[ Links ]
35. BUTTS, Christine A.; MOUGHAN, P.J. and SMITH, William C. Endogenous amino acid
flow at the terminal ileum of the rat determined under conditions of peptide alimentation.
En: Journal of the Science of Food and Agriculture. 1991. vol. 55, no, 2, p.175187.
[ Links ]
36. HESS, V. and SVE, B. Effects of body weight and feed intake level on basal ileal
endogenous losses in growing pigs. En: Journal of Animal Science. 1999. vol. 77, no. 12,
p.3281-3288.
[ Links ]
37. CERVANTES RAMIREZ, Miguel, et al. Prdida de aminocidos endgenos en cerdos con
niveles variables de consumo de alimento. En: Agrociencia. Noviembre-diciembre, 2000.
vol. 34, no. 6, p. 707-715.
[ Links ]
38. LIDLLE, A.R. Proteins but not amino acids, carbohydrates, or fats stimulate
cholecystokinin secretion in the rat. En: American Journal of Physiology. August, 1986. vol.
251, no. 2, parte 1, p.G243-G248.
[ Links ]
39. OWSLEY, Walter F.; KNABE D.D. and TANKSLEY, T.D. Effect of sorghum particle size on
digestibility of nutrients at terminal ileum and over the total digestive tract of growingfinishing pigs. En Journal of Animal Science. March, 1981. vol. 52, no. 3, p.557566.
[ Links ]
40. LI, S. and SAUER, William C. The effect of dietary fat content on amino acid digestibility
in young pigs. En: Journal of Animal Science. 1994. vol. 72, no. 7, p.17371743.
[ Links ]
41. BARTH, Christian A., et al. Soybean trypsin inhibitor(s) reduce absorption of exogenous
and increase loss of endogenous protein in miniature pigs. En: Journal of Nutrition.
December, 1993. vol. 123, no. 12, p.2195-2200.
[ Links ]
42. GRANT, George and DRIESSCHE, Edilbert. Legume lectins: physiochemical and
nutritional properties. En: Recent advances of research in antinutritional factors in legume
seeds. 2 ed. Wageningen, The Netherlands, 1993. p.219-234.
[ Links ]
43. JANSMAN, A.J.M., et al. Effects of hulls of faba beans (Vicia faba) with low or high
content of condensed tannins on the apparent ileal and fecal digestibility of nutrients and
excretion of endogenous protein in ileal digesta and feces of pigs of pigs. En: Journal of
Animal Science. 1975. vol. 73, no. 1, p.118-127.
[ Links ]
44. JANSMAN, A.J.M. Tannins in feedstuffs for single- stomached animals. En: Nutrition
Research Reviews. 1993. vol. 6, p.209-236.
[ Links ]

45. HUISMAN, J. and JANSMAN, A.J.M. Dietary effects and some analytical aspects of
nutritional factors in peas (Pisum sativum), beans (Phaseolus vulgaris) and soybean
(Glycine max L.) in monogastric farm animals. A literature review. En: Nutrition Abastract
Review. 1991. vol. 61, p.901-921.
[ Links ]
46. MOSENTHIN, Rainer; SAUER, William C. and AHRENS, Frank. Dietary pectin's effect on
ileal and fecal amino acids digestibility and exocrine pancreatic secretions in growing pigs.
En: Journal of Nutrition. August, 1994. vol. 124, no. 8, p.1222-1229.
[ Links ]
47. LOW, A.G. Nutrient absorption in pigs. En: Journal of the Science of Food and
Agricultura. November, 1980. vol. 31, no. 11, p.1087-1130.
[ Links ]
48. SOHN, K.S., et al. Improved soybean proteins sources for early-weaned pigs: II. Effects
on ileal amino acids digestibility. En: Journal of Animal Science. 1994. vol. 72, no. 3, p.631637.
[ Links ]
49. JUST, A.; JORGENSEN, H. and FERNANDEZ, J.A. The digestive capacity of the caecumcolon and the value of the nitrogen absorbed from the hindgut for proteins syntesis in pigs.
En: British Journal of Nutrition. July, 1981. vol. 46, no. 1, p.209-219.
[ Links ]
50. INBEAH, M., and SAUER, W.C. The effect de dietary level of fat on amino acid
digestibilities in soybean meal and canola meal and rate of passage in growing pigs. En:
Livestock Production Science. 1991. vol. 29, p.227-239.
[ Links ]
Corporacin Universitaria Lasallista

Carrera 51 118 Sur 57

Caldas (Antioquia, Colombia)
PBX: (57-4) 300 02 00 ext 127, 136
Fax: (57-4) 300 02 00 ext 184
revistainvestigacion@lasallista.edu.co

Sites of nutrient digestion in growing pigs: Effect

of dietary fiber
1

1.
2.
3.
4.
5.

A. Wilfart*,
L. Montagne,
P. H. Simmins,
J. van Milgen* and
J. Noblet*,2

+ Author Affiliations
1.

INRA, UMR1079 Systmes dElevage Nutrition Animale et Humaine, F-35590

Saint Gilles, France;
2. Agrocampus Rennes, UMR1079 Systmes dElevage Nutrition Animale et
Humaine, F-35590 Saint Gilles, France; and
3. Danisco Animal Nutrition, Marlborough Wiltshire, SN8 IXN, United Kingdom
1.

Corresponding author: Jean.Noblet@rennes.inra.fr

Next Section

Abstract
The impact of dietary fiber on fecal digestion is well-known and provides a
comprehensive approach toward nutrient digestibility and availability. Little
quantitative information is available on digestion of fiber in the different segments of
the gastrointestinal tract (GIT). The objectives of this study were to obtain a method
allowing the quantification of the digestive process in different segments of the GIT
and to study the impact of dietary fiber on nutrient digestibility. Six barrows (average
initial BW of 30 kg and fitted with a simple T-cannula at the proximal duodenum and
caudal ileum) were used in a replicated 3 3 Latin square design. In each period, pigs
were offered 1 of 3 diets differing in fiber content (low, medium, and high). Differences
in fiber content were created by replacing wheat and barley with wheat bran. Titanium
dioxide was included in the diet as an indigestible marker to determine the apparent
digestibility coefficients in different segments of the GIT. The apparent digestibility of
ash, CP, DM, and OM increased in the different segments of the GIT. Duodenal
digestibility coefficients were negative for ash (e.g., 39.9% for the medium-and highfiber diets), indicating important endogenous mineral secretions by the stomach and
digestive glands. The duodenal digestibility of other nutrients and OM were positive
but close to zero and numerically lower in the diets with the greater fiber contents. The
fiber content in the diet did not affect the apparent ileal digestibility of nutrients.
Increasing the fiber content in the diet affected the fecal digestibility of CP, ether
extract, and energy (P < 0.01). The method used for studying sites of digestion in the
digestive tract provides promising results, but it is limited due to the high variability
that is likely caused by sampling limitations and variation between animals.

dietary fiber

digestion

endogenous secretion

pig

Previous SectionNext Section

INTRODUCTION

Feed formulation is based on the principle that nutritional values of feed ingredients
are additive. However, it is known that digestibility is affected by physical and
chemical characteristics of the feed (Le Goff and Noblet, 2001), dietary supplements,
feed processing (Lahaye et al., 2004), animal factors, and feeding level (Noblet and
Shi, 1994). In addition, the type and site of digestion (i.e., enzymatic digestion in the
small intestine and fermentation in the large intestine) will determine the type of
nutrients that are absorbed. Although considering digestibility as a single (ileal or
fecal) characteristic is of practical importance, it cannot account for interactions
among nutrients or for interactions between the animal and nutrients.
Mathematical modeling is a method for integrating theories and observations to obtain
a comprehensive view of complex biological systems (Sauvant, 1992). To our
knowledge, only 3 models describing ileal or total tract digestion have been developed

for pigs (Usry et al., 1991; Bastianelli et al., 1996; Rivest et al., 2000). Digestion is an
integrated process of hydrolysis, absorption, fermentation, secretion, and transit. The
importance of each of these processes depends on the type and quantity of nutrients
supplied, and on the site of digestion. Dietary fiber is known to influence several
aspects of the digestive processes (Noblet and Perez, 1993). However, there is
relatively little quantitative information on digestibility and transit in different
segments of the gastrointestinal tract (GIT).
The objectives of the current study were to quantify the contributions of stomach,
small intestine, and large intestine to total tract nutrient digestibility, and also to
determine the impact of dietary fiber content on passage rates of nutrients in these
segments according to dietary fiber content. The present paper presents the
digestibility results.
Previous SectionNext Section

MATERIALS AND METHODS

Diets and Feeding
Three experimental diets based on wheat, barley, soybean meal, and wheat bran were
formulated (Table 1). Diets with different dietary fiber contents were created by partly
replacing wheat and barley by wheat bran. The low- (LF), medium- (MF), and highfiber (HF) diets contained 17, 21, and 27% of total dietary fiber, respectively. Rapeseed
oil was used to equalize the lipid content in the diets (2.5%). Titanium dioxide (0.3%)
was included as an inert marker for digestibility calculations. The diets were offered to
the pigs as pellets.
View this table:

In this window
In a new window

Table 1.
Formulation and chemical composition of the experimental diets
All pigs were offered the same quantity of feed for a given week, which corresponded
to approximately 80 g of DM (kg of BW) 0.60d1. This quantity was adjusted weekly. The
ration was distributed in 6 equal portions every 4 h using an automatic feeder. Water
was available ad libitum throughout the experiment. Feed refusals and spillage, if any,
were collected daily and analyzed for DM content.

Animals, Experimental Design, and Digesta Collection

All pigs came from the herd of the Institut National de la Recherche Agronomique
(Saint-Gilles, France). The care and use of animals were performed according to the
Certificate of Authorization to Experiment on Living Animals provided by the French
Ministry of Agriculture. Two blocks of 3 littermate barrows [Pietrain (Large White
Landrace)] were used. At approximately 33 kg of BW, pigs were fitted with simple Tcannula at the proximal duodenum (20 cm caudal to the pylorus; i.e., just caudal to the
pancreatic and biliary ducts), and in the caudal ileum according to procedures adapted
from Sauer et al. (1983). The silicone cannulas had internal diameters of 1.3 and 1.7
cm for duodenum and ileum, respectively. Prior to the use of halothane anesthesia,
pigs were sedated with an i.m. injection of ketamine. After surgery, pigs were
individually housed in metabolism crates in a temperature-controlled room (23 1C),

and were allowed a 2-wk recovery period. During this period, feed allowance was
increased gradually to attain 1.7 kg/d at the end of the recovery period.
Each block of pigs was used in a 3 3 Latin square design, using a different diet in
each period. Experimental periods lasted 14 d each, and pigs were weighed weekly.
The first week of each period was used to adapt the animals to the diet and to take
duodenal and ileal samples to be used for the determination of nutrient digestibility
(i.e., the objective of the current paper). The second week was used to determine
transit kinetics by feeding the animals a single marked meal (data not shown).
On d 6 and 7 of each experimental period, samples of duodenal and ileal digesta were
collected 3 times (at 0900, 1200, and 1730) in sterilized plastic bags (Whirl-pak, Nasco,
Fort Atkinson, WI). The total quantity of digesta collected (approximately 120 g as fresh
material) represented about 1% of the DM intake. Fecal samples were collected during
a 13-h period (from 0730 to 2030) on d 10. Duodenal, ileal, and fecal samples were
weighed and frozen (20C) immediately after collection. Before analysis, samples
were freeze-dried and finely ground. Samples from each collection day (3 samples/d)
were pooled by animal (within period and diet) and stored at 4C. After the
experiment, pigs were euthanized, and an autopsy was performed to evaluate the
tissue around the cannula.

Analytical Methods
Laboratory analyses were carried out on feed, duodenal and ileal digesta, and fecal
samples for each animal. Diets were analyzed for DM, OM, and ether extract (AOAC,
1990). Crude protein (N 6.25) was analyzed according to the Dumas method (AOAC,
1990), and GE was measured using an adiabatic bomb calorimeter (IKA, Staufen,
Germany). Fiber fractions (NDF, ADF, and acid-detergent lignin) of diets were
determined according to the method of Van Soest and Wine (1967), using a sequential
procedure with prior amylolytic treatment. Total dietary fiber (TDF) and insoluble fiber
were determined according to the method of Prosky et al. (1985). Soluble fiber was
estimated as the difference between TDF and insoluble fiber. Starch content was
measured using an enzymatic method (Thivend et al., 1965). The concentration of
titanium dioxide in diets, digesta, and feces was determined photometrically (Cobas
Mira, HORIBA ABX, Montpellier, France) according to the method described by Njaa
(1961). Fecal samples were analyzed for DM, OM, CP, ether extract (after acid
hydrolysis), GE, and the fiber fractions, as described before for feed samples. Because
of the limited availability of samples, starch, TDF, and insoluble dietary fiber contents
were measured only in ileal samples, whereas DM, ash, and CP were analyzed in
duodenal and ileal samples as described previously.

Calculations and Statistical Analyses

The apparent duodenal, ileal, and fecal digestibility of nutrients and energy was
calculated using the nutrient-to-marker ratio in the diet and digesta or feces according
to the following equation:

where Z and Zdiet are the nutrient (or energy) concentrations in digesta (or feces) and in
the diet, respectively; and TiO2 and TiO2, diet represent the concentration of titanium
dioxide in digesta (or feces) and in the diet, respectively. In this calculation,
digestibility refers to the cumulative digestibility at the end of each digestive segment
(i.e., duodenal, ileal, and fecal digestibility). Apparent digestibility was also calculated
for each digestive segment relative to the nutrient and energy supply to that segment.

In addition, nutrient concentrations in digesta were calculated relative to 100 g of DM

intake. Expressing the results as concentrations (nutrient per 100 g of DM intake)
makes it possible to partly overcome the differences in the nutrient contents between
the diets. It also allows quantifying of the contribution of each nutrient to the overall
flow of DM.
Data were analyzed according to the GLM procedure (SAS Inst. Inc., Cary, NC).
Experimental period (n = 3), diet (n = 3), and pig (n = 6) were included in the
statistical model. Results are presented as least squares means with residual standard
deviation (RSD). The RSD is the root mean square of the residual error and applies to
the whole model, not an individual estimate within the model. Contrasts were used to
determine differences between treatments.
Previous SectionNext Section

RESULTS

One of the pigs was removed from the statistical analysis for the third period because
of lack of appetite during this period. All other pigs appeared healthy during the
experiment, and diets were readily consumed. The BW of the pigs was not affected by
the diet and averaged 38, 48, and 59 kg during the 3 successive periods, which
corresponds to an average daily gain of 757, 686, and 606 g/d, respectively. The
average consumption of water by pigs was 2.7, 3.1, and 3.4 L/d for the LF, MF, and HF
diets, respectively; these values were not statistically different. Autopsy of the pigs did
not reveal complications of the surgical procedure. Duodenal and ileal cannulae were
positioned 18 cm from the pylorus and 17 cm prior to the ileocecal valve, respectively.
Visual observation of the digestive tract did not reveal disorders, and cicatrisation
around the cannula was not excessive.
Apparent digestibility of most nutrients increased along the GIT from the duodenum
onwards (Table 2). For all diets, duodenal ash digestibility was negative (45.0,
39.9, and 39.9% for the LF, MF, and HF diets, respectively). According to the ash
content of the diets, this corresponds to apparent endogenous ash secretions of 2.5
and 2.8 g/100 g of DM intake for the LF and HF diets, respectively. The ash flow
entering the duodenum was 40% larger than the ash intake (Table 3) and indicates
the importance of endogenous mineral secretions prior to the duodenum (e.g., due to
saliva and gastric secretions). Apparent digestibility of dietary ash increased along the
gut and was positive at the end of the ileum. Fecal ash digestibility ranged from 40 to
50%. Dietary fiber did not affect duodenal or ileal ash digestibility, but affected (P =
0.01) fecal ash digestibility with decreased values for HF diet compared with the LF
diet (43.4 vs. 51.3%).
View this table:

In this window
In a new window

Table 2.
Effect of the fiber content in the diet on apparent duodenal, ileal, and fecal digestibility
of dietary components1
View this table:

In this window
In a new window

Table 3.
Effect of the fiber content in the diet on the concentration of components in the feed,
at the beginning of the duodenum, at the end of the ileum, and in the feces1
The apparent CP digestibility was low at the proximal duodenum for all diets (15, 12,
and 7% for LF, MF, and HF diets, respectively) and was not affected by the diet
composition. As anticipated, apparent ileal and fecal CP digestibilities were largely
positive, averaging 73 and 84% for the 3 diets, respectively. Apparent ileal digestibility
of CP was not affected by fiber content, but fecal CP digestibility was lower (P < 0.01)
in fiber-rich diets (81.3% for HF vs. 87.3% for LF). The results for the ileal TDF
digestibility were negative for LF and MF diets (31 and 5%, respectively), but
positive for HF diet. Fecal apparent TDF digestibility was positive for all diets. Virtually
all starch was digested at the end of the small intestine, and digestibility was not
affected by the diet. No starch could be detected in a few fecal samples that were
analyzed for verification. Fecal digestibility of ether extract decreased (P < 0.01) with
increasing dietary fiber content (77.0 vs. 65.2% for LF and HF diets, respectively).
For OM, the duodenal, ileal, and fecal digestibilities followed the trends seen for the
individual nutrients. Apparent digestibility was modest up to proximal duodenum and
increased in the subsequent segments of the digestive tract. In association with a
negative duodenal apparent digestibility of ash, duodenal digestibility of DM was
reduced compared with OM digestibility and was decreased to the extent that negative
values were observed for some pigs offered the HF diet. Moreover, increasing the fiber
content of the diet decreased the fecal OM digestibility (P < 0.01), had no effect on
ileal digestibility, and tended to decrease (P = 0.10) the duodenal OM digestibility.
Energy digestibility followed a pattern similar to that of DM or OM (P < 0.01). There
was a pig effect (P = 0.03) for fecal digestibility of DM, OM, TDF, ash, and a tendency
(P = 0.09) for CP but not for duodenal and ileal digestibility, indicating an individual
specificity of the digestion process at the fecal stage. There was no period effect for
any of the measured criteria.
The nutrient flows of digesta in the different segments of the GIT relative to DM intake
are presented in Table 3. Except for ether extract, nutrient concentrations were
different in the experimental diets. As indicated by the digestibility results, the
duodenal flow of ash was greater than the intake, implying apparent endogenous
secretions equivalent to approximately 2.7 g of ash per 100 g of DM intake; this value
was not affected by the dietary fiber content. The (numerical) differences among diets
for ash flow at the proximal duodenum were absent at the ileum and the rectum. Flows
of CP, starch, ether extract, and TDF at the duodenum and the ileum were not affected
by the diet. However, flows of CP, ether extract TDF, and of OM and DM were greater
(P < 0.01) for HF compared with LF diets at the rectum. For instance, the calculated
rate of absorption in the large intestine was almost 2 times as high for the LF diet as
for the HF diet (20.8 vs. 11.2 g per 100 g of DM intake; Table 3). Finally, data in Table
3 indicated that the DM excreted at the rectum was mainly composed of TDF (50 to
60%) and that the increased fecal DM excretion observed for the HF diet was mainly
due to increased TDF excretion.
Previous SectionNext Section

DISCUSSION

The in vivo method used in the current study allows the quantification of digestion at
the proximal duodenum, the terminal ileum, and the rectum in the same animal.
Although the multicannulation technique has been used in ruminants (Faichney, 1975;
Siddons et al., 1985; Faichney, 1993) and preruminant calves (Montagne et al., 2001),
it has only been used in few studies with pigs. For pigs, digestion has been studied
frequently at the rectum (Darcy-Vrillon et al., 1991; Kavanagh et al., 2001; Le Goff et
al., 2002) and to a lesser extent at the terminal ileum (Shi and Noblet, 1993;

Buraczewska, 2001; Souffrant, 2001). In the case of amino acids for which ileal
digestibility has to be measured, ileal T-cannula or ileo-rectal anastomosis have been
mainly used. The ileo-rectal anastomosis has the disadvantage that the cecum and
colon will cease to function and that special diets are required to maintain animals in
good health. The present technique expands on that of using the ileal T-cannula in a
way that the contribution of the stomach (and pancreas and liver) can be separated. It
is evident that this technique requires a more significant surgical intervention. For ease
of sampling, it is also important that the pigs get accustomed to human intervention.
Nevertheless, the method has some limitations, one of these being the high variability
of the results. In Table 2, the RSD was much greater for the duodenal and ileal
digestibility results compared with the fecal digestibility data. The variability among
animals is known to contribute to the overall high variability of ileal digestibility
estimates (Van Leeuwen et al., 1996). The main reason for this is that considerably
smaller quantities of samples are obtained from the duodenum and ileum
(approximately 13 g of DM each) compared with fecal samples (270 g of DM). The use
of T-cannulas involves a partial collection of digesta (Fuller et al., 1994), and the
method has been criticized because of the small quantities of digesta taken and the
possibility that collected samples are not representative of the total digesta
(Titgemeyer, 1997). Furthermore, the presence of the cannula may alter the normal
passage of digesta as suggested by Radcliffe et al. (2005), which may result in
perturbations of digestive processes after the cannula. Furthermore, Yin et al. (2000)
suggested that the small diameter of T-cannula may induce a change in pressure at
the base of the cannula when it is opened. This could result in separation of the larger
and finer particles, an effect that may be greater for diets rich in fiber. Furthermore, as
gastric emptying follows a pulsatory pattern, it is not known if the sample is taken at
the beginning, the middle, or the end of the pulse. Moore (1959) suggested that
variability in duodenal digestibility depended on the interval between feeding, the
individual pig, and the duration of eating. In our study, the interval between feedings
(every 4 h) and the duration of eating were regular and similar for the pigs, and it can
be hypothesized that ileal digesta passage was relatively constant (Van Leeuwen et al.,
1997). This highlights the suggestion that the observed variability is inherent to the
individual animal. Although not significant, the probabilities for an individual pig effect
were lower for the duodenal than for ileal digestibility (Table 2) and may suggest that
endogenous secretions were affected by the animal. These observations also indicate
that duodenal and ileal sample sizes should be increased to attenuate this
methodological variability.
A rather surprising result was the negative apparent ileal digestibility of TDF with the
LF diet, and to a smaller extent, with the MF diet. This indicates that more TDF was
measured at the ileum than in the feed. Similar results have been obtained by other
authors also using wheat bran as a source of fiber (Graham et al., 1986; Jorgensen et
al., 1996). It has been suggested that contamination with endogenous and microbial
matter may contribute to the polysaccharide content of the sample (Graham et al.,
1986; Jorgensen et al., 1996). The method of Prosky et al. (1985), which is a
gravimetric method, may be sensitive to this contamination, resulting in an artificial
increase in fiber content and underestimation of fiber digestion. Thus, the rather
surprising result for the ileal digestibility of TDF may have originated from the
combination of sampling or analytical errors and the relatively high variability of
results. The results for ileal digestibility of OM were also surprising. Indeed, the
enrichment of fiber in the diet was achieved by a replacement of starch with fiber.
Taking into account the high digestibility of starch at the ileum, it can be anticipated
that diets with a low fiber content (and thus with a high starch content) are more
digestible than those having a high fiber content. However, our results showed that
there is no effect of fiber on ileal digestibility of OM. This finding is inconsistent with
literature data (Shi and Noblet, 1994; Leming and Lindberg, 2001; Hgberg and
Lindberg, 2004). Also, the fiber content in the diet did not affect CP digestibility, which
is not consistent with results reported by Owusu-Asiedu et al. (2006). This absence of

an effect of fiber on OM and CP apparent digestibility might be partly explained by the

negative digestibility of fiber at the ileum.
Digestion of nutrients begins soon after ingestion of the diet, and digestibility becomes
greater along the gut. However, the apparent duodenal digestibility of ash was
negative (Table 2), indicating a secretion of endogenous material prior to the
cannula. Apparent ash digestibility became positive at the end of ileum. Because the
duodenal cannula was positioned just after the entrance of the pancreatic and biliary
ducts, the samples of duodenal digesta collected presumably contained endogenous
secretions from the pancreas and liver in addition to saliva and gastric secretions. The
apparent duodenal digestibility of CP was low but positive. These low values are the
result of a combination of 2 processes. First, there is an endogenous input in the form
of lumen of proteins (e.g., mucins, enzymes, and proteins from desquamated cells)
originating from the mouth, esophagus, stomach, proximal duodenum, pancreas, and
liver. Also, hydrolysis of protein and absorption of amino acids may start at the
stomach (Buraczewska, 1981) or immediately after the stomach with a subsequent
disappearance of CP from proximal duodenum. The apparent duodenal CP digestibility
ranged from 7% (HF) to 14% (LF), illustrating that the digestion and absorption of
dietary CP is greater than the endogenous secretions before the proximal duodenum.
For growing pigs, Souffrant (1991) estimated the endogenous N secretion from saliva
to be 0.22 g/d, whereas Corring (1980) estimated it to be 0.40 g/d. Estimates of gastric
N secretion range between 2.0 (Souffrant, 1991) to 3.3 g/d (Simon et al., 1986). Other
sources include pancreatic (2.5 to 6.7 g of N/d; Souffrant, 1991) and biliary secretions
(1.9 to 3.0 g of N/d; Sambrook, 1978; Juste, 1982). According to Zebrowska and
Kowalczyk (2000), the total N secretion in the stomach and proximal duodenum is
approximately 9 g/d in 30-kg pigs or 20 to 25% of the dietary protein intake.
Furthermore, the endogenous N secretion depends on the presence and nature of
dietary fiber, and to a lesser extent, on the quantity of feed (Souffrant, 1991;
Zebrowska and Kowalczyk, 2000). Our study did not confirm these values but indicated
a nonnegligible absorption of N compounds before the proximal duodenum. Other
methods (e.g., isotopes techniques) or cannulation at other sites would have been
necessary to quantify these aspects (Lahaye et al., 2004).
In agreement with the results of Noblet and Perez (1993) and Le Goff and Noblet
(2001), increasing the fiber content in the diet decreased the apparent fecal
digestibility of nutrients and OM. Moreover, the measured fecal digestibility of OM and
energy was similar to the digestibility values calculated from the feed ingredients
(Sauvant et al., 2004). The decrease in fecal ash and CP observed for the HF diet
compared with the LF diet (Table 2) could be the result of a specific digestive
processes due to the increased fiber content. In fact, a lower apparent digestibility can
be explained by increased endogenous secretions, or a decreased hydrolysis and
absorption of nutrients, or both. Wheat bran, which was the major fiber source in our
trial, is relatively resistant to microbial degradation (Stephen and Cummings, 1980;
Donangelo and Eggum, 1985), resulting in an increase in fecal dry matter and fecal
bulk (Bach Knudsen and Hansen, 1991). Consequently, because of its physical
presence (40% for the HF diet), wheat bran is one of the most effective dietary fiber
sources for increasing the rate of passage in the digestive tract (Jorgensen et al.,
1996). Digestion in the hindgut is affected by the time that the digesta is subjected to
fermentation, and a rapid passage of digesta may diminish the effectiveness of this
process (Morel et al., 2006). This can be a factor that partially explains the decrease of
fecal digestibility in association with the increase of dietary fiber. Similar observations
have been reported by Hgberg and Lindberg (2004) who compared fecal digestibility
of diets containing cereals or high- and insoluble-fiber (30% wheat bran).
The stomach, small intestine, and large intestine do not have the same implication in
the digestive process, and their contribution differs depending on the nutrient
considered. If endogenous secretions are ignored, the large intestine seems to be the
major site of mineral absorption (54 vs. 25% before the end of the ileum). However,

because of the important secretion of endogenous minerals before the duodenal

cannula, and in agreement with the results of Partridge (1978), the small intestine is in
fact a major site of absorption of mineral arriving in the duodenum (40 vs. 33% in the
large intestine). According to published data, different minerals are absorbed at
different sites. Calcium and P are absorbed in the first half of the small intestine, Na in
the ileum and the colon, Mg only in the colon, and K is absorbed in all regions of the
digestive tract (Partridge, 1978). The effect of dietary fiber on the contribution of small
and large intestine on ash absorption was not significant.
In addition to its role in the secretion of minerals, the segment prior to the proximal
duodenum has a role in the hydrolysis and absorption of proteins. In the current study,
11% of CP was absorbed prior to the duodenum. In agreement with studies reported in
the literature (Dierick et al., 1983; Just et al., 1985; Shi and Noblet, 1993), the present
experiment also indicates that a large proportion of ingested CP (62%) is digested in
the small intestine, whereas only 12% of CP is digested in the large intestine.
Compared with the quantities of CP entering the small and large intestine, the
apparent digestibilities of CP were on average 69 and 49% in each segment,
respectively. These values are greater than results of Kass et al. (1980) who showed,
for alfalfa diets, an apparent CP digestibility of 48 to 69% for the small intestine, and
20 to 35% for the large intestine. In agreement with results of Shi and Noblet (1993),
the CP digestibility in the large intestine was reduced when the dietary fiber content is
increased in the current study. In fact, this may be indicative of ammonia flux toward
the large intestine due to the presence of fermentable OM. This would result in a shift
of N loss from the urine to the feces. Starch was totally digested at the end of the
ileum in our study and it can be assumed that most starch is digested in the ileum
(Bach Knudsen and Hansen, 1991; Jorgensen et al., 1996; Hgberg and Lindberg,
2004). It is generally assumed that dietary fat is digested before the end of the ileum
(Shi and Noblet, 1994) with some hindgut production of microbial fat (Shi and Noblet,
1993). Therefore, total tract digestibility of fat might then be lower than ileal
digestibility (Hgberg and Lindberg, 2004).
On average for the 3 diets, 13% of the dietary OM was digested before the proximal
duodenum, 52% in the small intestine (and thus 65% before the end of the ileum), and
17% in the large intestine. In other words, 16, 63, and 21% of the digested OM was
degraded before the proximal duodenum, in the small intestine, and in the large
intestine, respectively. The OM digestibility was lower than that of Shi and Noblet
(1993), who estimated that the contribution of the large intestine to OM digestibility
was 25%. The values obtained in the current study were greater than those observed
by Hgberg and Lindberg (2004) and Laplace et al. (1989). In fact, diet composition
seems to have a major effect on the contribution of the hindgut to the OM digestibility.
For example, Shi and Noblet (1993) obtained minimal and maximal contributions of 13
and 32%, respectively, and these values were obtained with low- (9.7% NDF) and highfiber diets (26% NDF).
In conclusion, the methodology used in this study allows the quantification of digestion
in different segments of the gastrointestinal tract using the same animal. There was a
high residual variability in the present experiment, especially for the duodenal and ileal
digestibility values. This variability might probably be reduced if greater quantities of
duodenal and ileal digesta are collected.
Previous SectionNext Section

Footnotes

1 The authors gratefully acknowledge A.-M. Debicki-Garnier and B. Messager for

their advice and contribution in the discussions,Y. Jaguelin-Peyraud, and A.
Pasquier for the laboratory analyses and Y. Lebreton, F. Le Gouevec, B. Janson, and
V. Piedvache for the animal care. This study was supported by CEVA Nutrition
Animale, Libourne (France), and Danisco Animal Nutrition (United Kingdom).

Received July 4, 2006.

Accepted November 9, 2006.

Copyright 2007 Journal of Animal Science

Previous Section

LITERATURE CITED
1.
AOAC. 1990. Official Methods of Analysis. 15th ed. Assoc. Off. Anal. Chem.,
Arlington, VA.
2.
Bach Knudsen, K., and I. Hansen. 1991. Gastrointestinal implications in pigs of
wheat and oat fractions. 1. Digestibility and bulking properties of
polysaccharides and other major constituents. Br. J. Nutr. 65:217232.
CrossRefMedline
3.
Bastianelli, D., D. Sauvant, and A. Rrat. 1996. Mathematical modeling of
digestion and nutrient absorption in pigs. J. Anim. Sci. 74:18731887.
Abstract/FREE Full Text
4.
Buraczewska, L. 1981. Absorption of amino acids in different parts of the small
intestine in growing pigs. 3. Absorption of constituents of protein hydrolysates.
Acta Physiol. Pol. 32:569584.
Medline
5.
Buraczewska, L. 2001. Fibre components negatively affect ileal protein
digestibility in pigs. J. Anim. Feed Sci. 10:139152.
6.
Corring, T. 1980. Endogenous secretions in the pig. Pages 136150 in Current
Concepts of Digestion and Absorption in Pigs. A. G. Low, and I. G. Partridge, ed.
N.I.R.D. Reading, Shinfield, UK.
7.

Darcy-Vrillon, B., W.-B. Souffrant, J. Laplace, A. Rerat, T. Corring, P. Vaugelade,

G. Gebhardt, and R. Kohler. 1991. Exogenous and endogenous contributions to
nitrogen fluxes in the digestive tract of pigs fed a casein diet. 2. Ileal and
faecal digestibilities and absorption of amino acids. Reprod. Nutr. Dev. 31:561
573.
CrossRefMedline
8.
Dierick, N., J. Decuypere, J. Lannoye, I. Vervaeke, and H. Henderickx. 1983. Ileal
and faecal digestion of dry matter, protein and amino acids in some
conventional diets for fattening pigs. Rev. Agric. 36:17131726.
9.
Donangelo, C. M., and B. Eggum. 1985. Comparative effects of wheat bran and
barley husk on nutrient utilization in rats. 1. Protein and energy. Br. J. Nutr.
54:741751.
CrossRefMedline
10.
Faichney, G. 1975. The use of markers to partition digestion within the
gastrointestinal tract of ruminant. Pages 277291 in Digestion and Metabolism
in the Ruminant. I. W. MacDonald, and A. C. I. Warner, ed. The University of
New England, Sidney, New South Wales, Australia.
11.
Faichney, G. 1993. Digesta flow. Pages 5385 in Quantitative Aspects of
Ruminant Digestion and Metabolism. J. Forbes, and J. France, ed. CAB
International, Wallingford, UK.
12.
Fuller, M., B. Darcy-Vrillon, J. Laplace, M. Picard, A. Cadenhead, J. Jung, D.
Brown, and M. Franklin. 1994. The measurement of dietary amino acid
digestibility in pigs, rats and chickens: A comparison of methodologies. Anim.
Feed Sci. Technol. 48:305324.
13.
Graham, H., K. Hesselman, and P. Aman. 1986. The influence of wheat bran
and sugar-beet pulp on the digestibility of dietary component in a cereal-based
pig diet. J. Nutr. 116:242251.
Abstract/FREE Full Text
14.

Hgberg, A., and J. Lindberg. 2004. Influence of cereal non-starch

polysaccharides on digestion site and gut environment in growing pigs. Livest.
Prod. Sci. 87:121130.
15.
Jorgensen, H., X. Q. Zaho, and B. Eggum. 1996. The influence of dietary fibre
and environmental temperature on the development of the gastrointestinal
tract, digestibility, degree of fermentation in the hind-gut and energy
metabolism in pigs. Br. J. Nutr. 75:365378.
CrossRefMedline
16.
Just, A., H. Jorgensen, and J. A. Fernandez. 1985. Correlations of protein
deposited in growing female pigs to ileal and faecal digestible crude protein
and amino acids. Livest. Prod. Sci. 12:145159.
17.
Juste, C. 1982. Apports endognes par les scrtions digestives chez le porc.
Pages 155173 in Digestive Physiology in the Pig. J. Laplace, T. Corring, and A.
Rerat, ed. INRA, Versailles, France.
18.
Kass, M. L., P. J. Van Soest, W. G. Pond, B. Lewis, and R. E. McDowell. 1980.
Utilization of dietary fiber from alfalfa by growing swine. I. Apparent
digestibility of diet components in specific segment of the gastrointestinal
tract. J. Anim. Sci. 50:175191.
19.
Kavanagh, S., P. Lynch, F. OMara, and P. Caffrey. 2001. A comparison of total
collection and marker technique for the measurement of apparent digestibility
of diets for growing pigs. Anim. Feed Sci. Technol. 89:4958.
20.
Lahaye, L., P. Ganier, J. Thibault, and B. Seve. 2004. Technological processes of
feed manufacturing affect protein endogenous losses and amino acid
availability for body protein deposition in pigs. Anim. Feed Sci. Technol.
113:141156.
21.
Laplace, J. P., B. Darcy-Vrillon, J.-M. Perez, Y. Henry, S. Giger, and D. Sauvant.
1989. Associative effects between two fibre sources on ileal and overall
digestibilities of amino acids, energy and cell-wall components in growing pigs.
Br. J. Nutr. 61:7587.
CrossRefMedline

22.
Le Goff, G., J. Milgen, and J. Noblet. 2002. Influence of dietary fiber on digestive
utilization and rate of passage in growing pigs, finishing pigs and adult sows.
Anim. Sci. 74:503515.
23.
Le Goff, G., and J. Noblet. 2001. Comparative digestibility of dietary energy and
nutrients in growing pigs and adult sows. J. Anim. Sci. 79:24182427.
Abstract/FREE Full Text
24.
Leming, R., and J. Lindberg. 2001. Digestion of carbohydrates in fibre-rich diets
for pigs. Agraarteadus 12:210218.
25.
Montagne, L., R. Toullec, and J. P. Lalls. 2001. Intestinal digestion of dietary
and endogenous proteins along the small intestine of calves fed soyabean or
potato. J. Anim. Sci. 79:27192730.
Abstract/FREE Full Text
26.
Moore, J. H. 1959. The use of indicators in digestibility studies. Agric. Prog.
34:4863.
27.
Morel, P. C. H., T. S. Lee, and P. J. Moughan. 2006. Effect of feeding level, live
weigh and genotype on the apparent faecal digestibility of energy and organic
matter in the growing pig. Anim. Feed Sci. Technol. 126:6374.
28.
Njaa, L. R. 1961. Determination of protein digestibility with titanium dioxide as
indicator substance. Acta Agric. Scand. 11:227241.
29.
Noblet, J., and J. M. Perez. 1993. Prediction of digestibility of nutrients and
energy values of pig diets from chemical analysis. J. Anim. Sci. 71:33893398.
Abstract/FREE Full Text
30.

Noblet, J., and X. S. Shi. 1994. Effect of body weight on digestive utilization of
energy and nutrients of ingredients and diets in pigs. Livest. Prod. Sci. 37:323
338.
31.
Owusu-Asiedu, A., J. F. Patience, B. Laarveld, A. G. Van Kessel, P. H. Simmins,
and R. T. Zijlstra. 2006. Effects of guar gum and cellulose on digesta passage
rate, ileal microbial populations, energy and protein digestibility, and
performance of grower pigs. J. Anim. Sci. 84:843852.
Abstract/FREE Full Text
32.
Partridge, I. G. 1978. Studies on digestion and absorption in the intestines of
growing pigs 3. Net movements of mineral nutrients in the digestive tract. Br. J.
Nutr. 39:527537.
CrossRefMedline
33.
Prosky, L., N. Asp, I. Furda, J. DeVries, T. Schweizer, and B. Harland. 1985.
Determination of total dietary fiber in foods and food products: collaborative
study. J. Assoc. Off. Anal. Chem. 68:677679.
Medline
34.
Radcliffe, J. S., J. P. Rice, R. S. Pleasant, and G. A. Apgar. 2005. Technical note:
Improved technique for fitting pigs with steered ileocecal valve cannulas. J.
Anim. Sci. 83:15631567.
Abstract/FREE Full Text
35.
Rivest, J., J. F. Bernier, and C. Pomar. 2000. A dynamic model of protein
digestion in the small intestine of pigs. J. Anim. Sci. 78:328340.
Abstract/FREE Full Text
36.
Sambrook, I. E. 1978. Flox and composition of bile in growing pigs. Proc. Nutr.
Soc. 37:84A.
Medline
37.

Sauer, W., H. Jorgensen, and R. Berzins. 1983. A modified nylon bag technique
for determining apparent digestibilities of protein in feedstuffs for pigs. Can. J.
Anim. Sci. 63:233237.
38.
Sauvant, D. 1992. La modlisation systmique en nutrition. Reprod. Nutr. Dev.
32:217230.
CrossRefMedline
39.
Sauvant, D., J. M. Perez, and G. Tran. 2004. Tables of Composition and
Nutritional Value of Feed Materials: Pig, poultry, sheep, goats, rabbits, horses,
fish. Wageningen Academic Publishers, Wageningen, the Netherlands and INRA
Editions, Paris, France.
40.
Shi, X. S., and J. Noblet. 1993. Contribution of the hindgut to digestion of diets
in growing pigs and adult sows: effect of diet composition. Livest. Prod. Sci.
34:237252.
41.
Shi, X. S., and J. Noblet. 1994. Effect of body weight and feed composition on
the contribution of hindgut to digestion of energy and nutrients in pigs. Livest.
Prod. Sci. 38:225236.
42.
Siddons, R. C., J. Paradine, D. E. Beever, and P. R. Cornell. 1985. Ytterbium
acetate as a particulate-phase digesta-flow marker. Br. J. Nutr. 54:509519.
CrossRefMedline
43.
Simon, O., T. Zebrowska, R. Munchmeyer, H. Bergner, and H. Rohrmann. 1986.
Studies on the secretion of amino acids and urea into the gastro-intestinal tract
of pigs. 1. Secretion of leucine into the stomach and the upper part of
duodenum during continuous intravenous of 14C-leucine. Arch. Anim. Nutr.
36:516.
44.
Souffrant, W.-B. 2001. Effect of dietary fibre on ileal digestibility and
endogenous nitrogen losses in the pig. Anim. Feed Sci. Technol. 90:93102.
45.

Souffrant, W.-B. 1991. Endogenous nitrogen losses during digestion in pigs.

Pages 147166 in Digestive Physiology in Pigs. M. W. A. Verstegen, J. Huisman,
and L. A. den Hartog, ed. Wageningen (Doorwerth), the Netherlands.
46.
Stephen, A. M., and J. Cummings. 1980. The microbial contribution to human
faecal mass. J. Med. Microbiol. 13:4556.
Abstract/FREE Full Text
47.
Thivend, P., C. Mercier, and A. Guilbot. 1965. Dosage de lamidon dans les
milieux complexes. Ann. Biol. Anim. Biochim. Biophys. 5:513526.
48.
Titgemeyer, E. 1997. Design and interpretation of nutrient digestion studies. J.
Anim. Sci. 75:22352247.
Abstract/FREE Full Text
49.
Usry, J. L., L. W. Turner, T. S. Stahly, T. C. Bridges, and R. S. Gates. 1991. GI-tract
simulation model of the growing pig. Am. Soc. Agric. Eng. 34:18791890.
50.
Van Leeuwen, P., J. Doorenbos, K. McCracken, J. Ebbinge, and M. Verstegen.
1997. Digesta passage at the terminal ileum in pigs. Pages 531534 in
Digestive Physiology in Pigs. J. P. Laplace, C. Fevrier, and A. Barbeau, ed. EAAP
Publication No. 88. INRA, Paris, France.
51.
Van Leeuwen, P., A. Veldman, S. Boisen, K. Deuring, G. J. M. Van Kempen, G. B.
Derksen, M. W. A. Verstegen, and G. Schaafsma. 1996. Apparent ileal dry
matter and crude protein digestibility of rations fed to pigs and determinated
with use of chromic oxide (Cr2O3) and acid-insoluble ash as digestive markers.
Br. J. Nutr. 76:551562.
CrossRefMedline
52.
Van Soest, P. J., and R. H. Wine. 1967. Use of detergents in the analysis of
fibrous feeds. IV. Determination of plant cell-wall constituents. J. Assoc. Off.
Anal. Chem. 50:5055.
53.

Yin, Y.-L., J. D. G. McEvoy, H. Schulze, and K. J. McCracken. 2000. Studies on

cannulation method and alternative indigestible markers and the effects on
food enzyme supplementation in barley-based diets on ileal and overall
digestibility in growing pigs. Anim. Sci. 70:6372.
54.
Zebrowska, T., and J. Kowalczyk. 2000. Endogenous nitrogen losses in
monogastrics and ruminants as affected by nutritional factors. Asian-australas.
J. Anim. Sci. 13:210218.

Articles citing this article

Energy concentration and amino acid digestibility in corn and corn coproducts from
the wet-milling industry fed to growing pigs J ANIM SCI October 1, 2014 92:4557-4565
o
Abstract
o
Full Text
o
Full Text (PDF)
Relationships among dietary fiber components and the digestibility of energy,
dietary fiber, and amino acids and energy content of nine corn coproducts fed to
growing pigs J ANIM SCI October 1, 2014 92:4505-4517
o
Abstract
o
Full Text
o
Full Text (PDF)
Difference in short-term responses to a high-fiber diet in pigs divergently selected
for residual feed intake J ANIM SCI April 1, 2014 92:1512-1523
o
Abstract
o
Full Text
o
Full Text (PDF)
Effect of insoluble-low fermentable fiber from corn-ethanol distillation origin on
energy, fiber, and amino acid digestibility, hindgut degradability of fiber, and growth
performance of pigs J ANIM SCI November 1, 2013 91:5314-5325
o
Abstract
o
Full Text
o
Full Text (PDF)
Ileal flows and apparent ileal digestibility of fatty acids in growing gilts fed flaxseed
containing diets J ANIM SCI June 1, 2013 91:2729-2739
o
Abstract
o
Full Text
o
Full Text (PDF)
Metabolic effects of dietary sugar beet pulp or wheat bran in growing female pigs J
ANIM SCI February 1, 2012 90:523-532
o
Abstract
o
Full Text
o
Full Text (PDF)
Effect of fermentation of cereals on the degradation of polysaccharides and other
macronutrients in the gastrointestinal tract of growing pigs J ANIM SCI July 1, 2011
89:2096-2105
o
Abstract
o
Full Text
o
Full Text (PDF)
The site of intestinal disappearance of DL-methionine and methionine hydroxy
analog differs in pigs J ANIM SCI May 1, 2011 89:1385-1391

o
Abstract
o
Full Text
o
Full Text (PDF)
Effect of corn distillers dried grains with solubles and Eimeria acervulina infection on
growth performance and the intestinal microbiota of young chicks Poultry Science
May 1, 2011 90:958-964
o
Abstract
o
Full Text
o
Full Text (PDF)
Digestibility of dietary fiber in distillers coproducts fed to growing pigs J ANIM SCI
July 1, 2010 88:2373-2381
o
Abstract
o
Full Text
o
Full Text (PDF)
Evaluation of elevated dietary corn fiber from corn germ meal in growing female
pigs J ANIM SCI January 1, 2010 88:192-201
o
Abstract
o
Full Text
o
Full Text (PDF)
1.

Published online before print November 22, 2006, doi: 10.2527/jas.2006-431 J ANIM SCI April 2007 vol.
85 no. 4 976-983

1.

AbstractFree

2.

Full Text

3.

Full Text (PDF)