Chapter 4
Manganese Homeostasis in the Chick 1
2
2,3
L. Lee Southern, David H. Baker, and Kevin M. Halpin 1
Department of Animal Science, Louisiana Agricultural Experiment Station, Louisiana State University Agricultural Center, Baton Rouge, LA 70803 Department of Animal Sciences, University of Illinois, Urbana, IL 61801
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2
Manganese is a nutritionally important trace element for chicks. Dietary energy and protein sources contain very little bioavailable Mn, and these feed ingredients reduce the biopotency of inorganic Mn supplements. This adverse effect is exerted primarily in the intestine as a result of reduced Mn absorption and is mediated by the fiber and/or ash components of the feedstuffs. Gut absorption efficiencies are higher when a phytate-and fiber-free casein-dextrose diet is fed than when a corn-soybean meal diet is fed. Dietary i n terrelationships exist between Mn and Co and between Mn and Fe. Cobalt increases Mn absorption and may precipitate Mn toxicosis. Excess dietary Mn reduces Fe u t i l i z a t i o n , but excess Fe does not affect Mn utilization. Eimeria acervulina infection increases Mn absorption. Manganese n u t r i t u r e o f t h e c h i c k has been a f e r t i l e area o f i n v e s t i g a t i o n f o r over 50 y e a r s . Wilgus and a s s o c i a t e s (1) i n 1936 r e p o r t e d t h a t Mn would prevent p e r o s i s i n c h i c k s . Numerous r e s e a r c h p u b l i c a t i o n s have s i n c e expanded t h e knowledge o f Mn homeostasis i n t h e c h i c k . The c h i c k i s unique w i t h regard t o Mn. I t has a h i g h e r Mn requirement than i t ' s mammalian c o u n t e r p a r t , and t h e Mn a b s o r p t i o n e f f i c i e n c y i n c h i c k s i s thought t o be l e s s than i n mammals ( 2 ) . The purpose o f t h i s r e p o r t w i l l be t o review c u r r e n t a s p e c t s o f Mn homeostasis i n t h e c h i c k . In p a r t i c u l a r , Mn a b s o r p t i o n
^Current address: National Dairy Council,
6300
North River Road, Rosemont,
0097-6156/87/0354-0035$06.00/0 © 1987 American Chemical Society
Kies; Nutritional Bioavailability of Manganese ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
IL 60018
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NUTRITIONAL BIOAVAILABILITY OF MANGANESE
e f f i c i e n c y , s t o r a g e , t u r n o v e r , i n t e r a c t i o n s with o t h e r m i c r o m i n e r a l s and with macrominerals, e f f e c t o f c o c c i d i a l i n f e c t i o n s , requirement and t o x i c i t y , and b i o a v a i l a b i l i t y o f Mn i n convent i o n a l p o u l t r y feeds and i n i n o r g a n i c Mn supplements w i l l be addressed.
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B i o a v a i l a b i l i t y : F e e d s t u f f s and I n o r g a n i c Supplements Conventional P o u l t r y F e e d s t u f f s . Manganese i s one o f o n l y two o r t h r e e t r a c e elements t h a t must be supplemented t o c o n v e n t i o n al p o u l t r y d i e t s . T h i s requirement f o r supplementation n e c e s s i t a t e s knowledge o f Mn b i o a v a i l a b i l i t y i n p o u l t r y f e e d s t u f f s . Davis and coworkers (3) r e p o r t e d t h a t soybean p r o t e i n reduced Mn u t i l i z a t i o n , Holmes and Roberts (4) observed an i n c r e a s e d i n c i dence o f p e r o s i s i n c h i c k s f e d rapeseed meal and Seth and C l a n d i n i n (5) r e p o r t e d t h a t rapeseed meal n o t o n l y i n c r e a s e d t h e i n c i d e n c e o f p e r o s i s , but t h a t i t reduced t h e p e r o s i s - p r e v e n t a t i v e e f f i c a c y o f i n o r g a n i c Mn supplements. More r e c e n t l y , Hal p i n and Baker (6) concluded t h a t c o r n , soybean meal, f i s h meal, wheat bran and r i c e bran reduced Mn d e p o s i t i o n i n bone, b i l e and pancreas (Mn r e s p o n s i v e t i s s u e s ) when added t o a c a s e i n - d e x t r o s e d i e t c o n t a i n i n g 1000 ppm Mn. With t h e e x c e p t i o n o f r i c e bran, these f e e d i n g r e d i e n t s a l s o reduced t i s s u e Mn c o n c e n t r a t i o n s when t h e d i e t a r y supplemental l e v e l o f Mn was reduced t o 14 pom (the Mn requirement o f c h i c k s consuming c a s e i n - d e x t r o s e d i e t s ) . Rice bran p r o v i d e d b i o a v a i l a b l e Mn when t h e d i e t was a t o r below the c h i c k ' s Mn requirement. These experiments were conducted f o r two-week p e r i o d s and, although supplementation o f these f e e d i n g r e d i e n t s t o t h e c a s e i n - d e x t r o s e d i e t appeared t o reduce Mn a v a i l a b i l i t y , c h i c k g a i n and e f f i c i e n c y o f g a i n were n o t adv e r s e l y a f f e c t e d . In a subsequent seven-week i n v e s t i g a t i o n ( 7 ) , f i s h meal, wheat bran and a corn-soybean meal mixture ( 5 7 % corn and 43% soybean meal t o s i m u l a t e i n g r e d i e n t r a t i o s i n a 23% crude p r o t e i n d i e t ) reduced c h i c k performance and t i s s u e Mn conc e n t r a t i o n when added t o t h e c a s e i n - d e x t r o s e d i e t c o n t a i n i n g 14 ppm Mn. Only f i s h meal had a d e t r i m e n t a l e f f e c t when added t o a M n - d e f i c i e n t d i e t (7 ppm Mn). F i s h meal reduced g a i n , f e e d e f f i c i e n c y and t i s s u e Mn c o n c e n t r a t i o n s , and i t a l s o i n c r e a s e d the i n c i d e n c e and s e v e r i t y o f p e r o s i s . Wheat bran and t h e c o r n soybean meal m i x t u r e , however, i n c r e a s e d bone Mn c o n c e n t r a t i o n when added t o t h e d i e t c o n t a i n i n g 7 ppm Mn. These r e s e a r c h e r s concluded from t h e long-term i n v e s t i g a t i o n t h a t wheat bran and the corn-soybean meal mixture p r o v i d e d b i o a v a i l a b l e Mn when t h e c h i c k was t h r e a t e n e d with a Mn d e f i c i t , but not when t h e d i e t c o n t a i n e d adequate ( o r m a r g i n a l l y adequate) Mn. F i s h meal, on the o t h e r hand, c o n t a i n e d no b i o a v a i l a b l e Mn, r e g a r d l e s s o f Mn c o n c e n t r a t i o n i n t h e d i e t . Thompson and Weber (8) conducted a s i m i l a r i n v e s t i g a t i o n over a four-week p e r i o d u s i n g a soybean meal-dextrose basal d i e t . They added c e l l u l o s e ( 6 % ) , wheat bran ( 1 2 % ) , corn bran ( 9 . 7 % ) , soy bran ( 9 . 7 % ) , o a t h u l l s (7.3%) and r i c e bran (16.67%) t o t h e basal d i e t such t h a t f e e d i n g r e d i e n t a d d i t i o n s s u p p l i e d a p p r o x i m a t e l y 6% d i e t a r y n e u t r a l d e t e r g e n t f i b e r (NDF). These r e s e a r c h e r s concluded t h a t r i c e bran reduced
Kies; Nutritional Bioavailability of Manganese ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
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4.
SOUTHERN ET
AL.
Manganese Homeostasis in the
Chick
growth, f e e d e f f i c i e n c y and bone Mn c o n c e n t r a t i o n compared w i t h the basal d i e t . The o t h e r " f i b e r " sources d i d not a d v e r s e l y a f f e c t c h i c k performance o r bone and l i v e r Mn d e p o s i t i o n . These r e s u l t s d i f f e r s l i g h t l y from those o f H a l p i n and Baker ( 6 - 7 ) , but i n v e s t i g a t i o n a l d i s s i m i l a r i t i e s such as f i b e r c o n t e n t and Mn l e v e l i n the basal d i e t s probably account f o r the d i s c r e p a n c i e s . H a l p i n and Baker's d i e t c o n t a i n e d known amounts o f i n o r g a n i c Mn and was e s s e n t i a l l y d e v o i d o f f i b e r . Thompson and Weber's basal d i e t , however, c o n t a i n e d 3.8% n e u t r a l d e t e r g e n t f i b e r from soybean meal and 117 ppm Mn from a mixture o f both o r g a n i c and i n organic sources. Although minor d i f f e r e n c e s are e v i d e n t i n the r e s e a r c h des c r i b i n g Mn b i o a v a i l a b i l i t y , i t i s c l e a r t h a t most c o n v e n t i o n a l p o u l t r y f e e d s t u f f s c o n t a i n very l i t t l e b i o a v a i l a b l e Mn, and i n many c a s e s , they a c t u a l l y reduce a v a i l a b i l i t y o f i n o r g a n i c Mn supplements. The mechanism by which t h i s r e d u c t i o n i n a v a i l a b i l i t y occurs was r e c e n t l y e v a l u a t e d ( 9 ) . Chicks were f e d 2000 ppm Mn f o r 14 days and then p l a c e d on d i e t s c o n t a i n i n g 14 ppm Mn with o r without 10% wheat bran s u p p l e m e n t a t i o n . Chicks were k i l l e d s e r i a l l y f o r two weeks f o l l o w i n g the p e r i o d o f Mn " l o a d i n g " . T i s s u e Mn l e v e l s decreased with t i m e , but wheat bran d i d not a f f e c t r a t e o f t i s s u e Mn d e p l e t i o n . Thus, wheat bran d i d not a f f e c t homeostasis o f s t o r e d Mn. In another experiment ( 9 ) , 10% d i e t a r y wheat bran was f e d to c h i c k s r e c e i v i n g v a r y i n g amounts o f i n o r g a n i c Mn a d m i n i s t e r e d v i a i n t r a p e r i t o n e a l i n j e c t i o n . Wheat bran e r r a t i c a l l y a l t e r e d t i s s u e Mn c o n c e n t r a t i o n s , but i t s e f f e c t d i d not approach the magnitude and c o n s i s t e n c y o f t h a t o c c u r r i n g with o r a l Mn i n g e s t i o n . The s l i g h t l o w e r i n g e f f e c t o f d i e t a r y wheat bran on t i s s u e Mn d e p o s i t i o n i n c h i c k s r e c e i v i n g Mn v i a i n t r a p e r i t o n e a l i n j e c t i o n p r o b a b l y r e s u l t e d from wheat bran i n h i b i t i n g r e a b s o r p t i o n o f Mn o f b i l i a r y and p a n c r e a t i c o r i g i n . I t would seem, t h e r e f o r e , t h a t the gut i s the primary s i t e o f a c t i o n o f the adverse e f f e c t o f wheat bran on Mn homeos t a s i s i n the c h i c k . A subsequent experiment (9) was conducted to determine which chemical f r a c t i o n i n wheat bran, f i s h meal, r i c e bran and a corn-soybean meal mixture i s r e s p o n s i b l e f o r the reduced Mn a b s o r p t i o n . The n e u t r a l d e t e r g e n t f i b e r f r a c t i o n i n both wheat bran and the corn-soybean meal mixture reduced t i s s u e Mn conc e n t r a t i o n s t o the same e x t e n t as the i n t a c t f e e d i n g r e d i e n t s . However, the ash component was r e s p o n s i b l e f o r the Mn-lowering e f f e c t o f f i s h meal, and both the ash and n e u t r a l d e t e r g e n t f i b e r f r a c t i o n s o f r i c e bran reduced t i s s u e Mn c o n c e n t r a t i o n s , but not to the e x t e n t o f i n t a c t r i c e bran. T h i s s t u d y , although i n c o n c l u s i v e , i n d i c a t e s t h a t the f i b e r (NDF) component o f some f e e d s t u f f s and the mineral (ash) component o f o t h e r s have a n e g a t i v e impact on Mn homeostasis i n c h i c k s . Harmuth-Hoene and Schelenz (10) have r e c e n t l y r e v e a l e d a number o f p o s s i b l e mechanisms by which f i b e r c o u l d i n t e r f e r e with mineral absorpt i o n , van der Aar and a s s o c i a t e s (11) have a l s o r e p o r t e d t h a t d i e t a r y f i b e r reduces mineral a v a i l a b i l i t y i n c h i c k s .
Kies; Nutritional Bioavailability of Manganese ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
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NUTRITIONAL BIOAVAILABILITY OF MANGANESE
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Phytate has been s t u d i e d e x t e n s i v e l y with regard t o mineral (mostly Zn and Ca) s t a t u s o f a n i m a l s , and i t has been shown t o reduce whole-body Mn r e t e n t i o n i n r a t s (12). P h y t a t e , however, i s n o t p r e s e n t i n t h e n e u t r a l d e t e r g e n t f i b e r o r i n t h e ash component o f f e e d s t u f f s . T h e r e f o r e , phytate does not appear t o be r e s p o n s i b l e f o r t h e r e d u c t i o n o f Mn uptake i n c h i c k s f e d c o r n , soybean meal, wheat bran o r f i s h meal ( 9 ) . That phytate negat i v e l y impacts Mn n u t r i t u r e a l s o d i s a g r e e s with t h e r e s e a r c h o f Reinhold e t a_h ( 1 3 ) , who r e p o r t e d t h a t f i b e r , and n o t p h y t a t e , was t h e primary f a c t o r d e t e r m i n i n g b i o a v a i l a b i l i t y o f d i v a l e n t mineral elements i n breads. I n o r g a n i c Mn Supplements. The b i o a v a i l a b i l i t y o f i n o r g a n i c Mn supplements has been s t u d i e d l o n g e r and more e x t e n s i v e l y than the b i o a v a i l a b i l i t y o f Mn i n f e e d i n g r e d i e n t s . As e a r l y as 1939, G a l l u p and N o r r i s (14) added 50 ppm Mn as M n C l . 4 H 0 , MnS0 -4H 0, KMnO^, MnC0 o r as Mn0 t o a c o n v e n t i o n a l p o u l t r y d i e t and r e p o r t e d t h a t t h e d i f f e r e n t Mn sources were e q u a l l y e f f i c a c i o u s i n p r e v e n t i n g p e r o s i s i n c h i c k s . T h e i r high l e v e l o f Mn supplementation (50 ppm), however, may have p r e c l u d e d t h e p o s s i b i l i t y o f d e t e c t i n g small d i f f e r e n c e s between t h e compounds. Hennig and coworkers ( 1 5 ) , u s i n g uptake o f r a d i o l a b e l e d Mn l a t e r r e p o r t e d t h a t MnCL was more a v a i l a b l e t o t h e c h i c k than MnSO^ o r Mn0 . Watson e t a l . (16) i n 1970 d e s c r i b e d a growth and t i s s u e Mn uptake tecTirTique f o r a s s e s s i n g Mn b i o a v a i l a b i l i t y o f i n o r g a n i c supplements. These r e s e a r c h e r s subsequentl y r e p o r t e d (17) t h a t d i f f e r e n c e s i n Mn b i o a v a i l a b i l i t y e x i s t e d between d i f f e r e n t sources o f feedgrade Mn oxide and between f e e d grade and reagent-grade Mn c a r b o n a t e . Manganese o x i d e and Mn c a r b o n a t e , depending on t h e s o u r c e , however, were as a v a i l a b l e as M n S 0 ^ H 0 . In a d d i t i o n , these r e s e a r c h e r s r e p o r t e d t h a t bone Mn c o n c e n t r a t i o n was more r e f l e c t i v e o f d i e t a r y Mn c o n t e n t than growth o r bone ash p e r c e n t , and t h a t bone Mn c o n c e n t r a t i o n i n c r e a s e d i n c r e m e n t a l l y as d i e t a r y Mn c o n c e n t r a t i o n s i n c r e a s e d between 10 and 120 ppm. Southern and Baker (18) compared t h e b i o a v a i l a b i l i t y o f MnS0n.H 0, MnCL .4H 0, MnC0 and Mn0 by adding excess Mn (3000, 4000 o r 5000 ppm) t o a corn-soybean meal d i e t and then measuring t i s s u e Mn uptake, l i v e r Fe a c c u m u l a t i o n , blood hemoglobin and h e m a t o c r i t , as w e l l as growth and f e e d e f f i c i e n c y . From these d a t a , i t was concluded t h a t MnS0^.H 0, MnCL -4H 0 and MnC0 were more e f f i c a c i o u s sources o f Mn than Mn0 , and t h a t MnC0 was s l i g h t l y l e s s e f f i c a c i o u s than MnS0 .H 0 and MnCL -4H 0. Estimates o f b i o a v a i l a b i l i t y were made u s i n g t h e s l o p e - r a t i o t e c h nique. A s s i g n i n g a value o f 100% t o MnSO^.H-O, a v a i l a b i l i t y e s t i m a t e s were 102, 77 and 29% f o r MnCL .4H 0, MnCO^ and Mn0 , r e s p e c t i v e l y . Black and a s s o c i a t e s (19; used a s i m i l a r e x p e r i mental d e s i g n (1000, 2000 o r 4000 ppm excess Mn) and determined the b i o a v a i l a b i l i t y o f Mn i n MnO and MnC0 r e l a t i v e t o MnS0 .H 0. B i o a v a i l a b i l i t y e s t i m a t e s , again u s i n g t h e s l o p e - r a t i o t e c h n i q u e , were 32 and 60% f o r MnC0 and MnO, r e s p e c t i v e l y . S i m i l a r l y , Henry e t al_. (20) r e p o r t e d t h a t t h e Mn i n MnO was 66% a v a i l a b l e compare? with 100% f o r MnSO^.H-0. Manganese l e v e l s used i n t h i s i n v e s t i g a t i o n were 40, 80 and 120 ppm added t o a corn-soybean meal d i e t . 2
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Kies; Nutritional Bioavailability of Manganese ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
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4. SOUTHERN ET AL.
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T i s s u e Mn: Storage and
Manganese Homeostasis in the Chick
Turnover
Storage, From the d i s c u s s i o n o f Mn b i o a v a i l a b i l i t y , i t i s obv i o u s t h a t d i e t a r y Mn i n t a k e i s a c c u r a t e l y r e f l e c t e d i n t i s s u e Mn c o n c e n t r a t i o n i n the c h i c k . T h i s i s not s u r p r i s i n g i n t h a t most m i n e r a l s are d e p o s i t e d i n t o t a r g e t t i s s u e s to some degree. What i s s u r p r i s i n g , however, i s the remarkable c o n s i s t e n c y w i t h which increments o f d i e t a r y Mn, r e g a r d l e s s o f the c o n c e n t r a t i o n , are d e p o s i t e d i n t o c e r t a i n t i s s u e s . Southern and Baker (18,21) r e p o r t e d l i n e a r i n c r e a s e s i n bone and g a l l b l a d d e r Mn c o n c e n t r a t i o n i n c h i c k s f e d 0, 1500 o r 3000 ppm Mn (21) and i n b i l e conc e n t r a t i o n i n c h i c k s f e d 3000, 4000 o r 5000 ppm Mn (18). S i m i l a r l y , Black and coworkers (22) r e p o r t e d t h a t d i e t a r y s u p p l e ments o f 0, 1000, 2000 and 3000 ppm Mn l i n e a r l y i n c r e a s e d Mn c o n c e n t r a t i o n i n l i v e r , kidney, muscle, bone and plasma with c o r r e l a t i o n c o e f f i c i e n t s ( r ) o f .832, .933, .642, .974 and .893, r e s p e c t i v e l y . Black and coworkers (23) extended these f i n d i n g s to account f o r l e n g t h o f time o f Mn f e e d i n g ( e i t h e r 1, 2 o r 3 weeks). Chicks were f e d 0, 1000, 2000 o r 3000 ppm Mn and k i l l e d a t one, two o r t h r e e weeks a f t e r i n i t i a t i o n o f treatment d i e t s . M u l t i p l e r e g r e s s i o n a n a l y s i s a c c o u n t i n g f o r time o f Mn f e e d i n g and d i e t a r y Mn c o n c e n t r a t i o n r e v e a l e d l i n e a r i n c r e a s e s i n l i v e r (.915), kidney (.980), pancreas (.931), muscle (.945), bone (.987) and plasma (.969) Mn c o n c e n t r a t i o n s ( c o r r e l a t i o n s c o e f f i c i e n t s in parentheses). T i s s u e Mn c o n c e n t r a t i o n s are not o n l y r e s p o n s i v e to high d i e t a r y Mn l e v e l s , but a l s o t o d i e t a r y Mn l e v e l s near the c h i c k ' s requirement. Watson and coworkers (16-17) r e p o r t e d t h a t bone Mn responded l i n e a r l y to d i e t a r y supplements o f 0 t o 120 ppm Mn. T h i s f i n d i n g was l a t e r confirmed by Southern and Baker (21) and by Henry e t aj_. ( 2 0 ) , and the r e s p o n s i v e t i s s u e s were expanded t o include~"bone and kidney. Remarkably, s l o p e ( t i s s u e Mn concent r a t i o n r e g r e s s e d on Mn i n t a k e ) was the same between 0 and 100 ppm d i e t a r y Mn as t h a t o c c u r r i n g between 100 and 1000 ppm Mn. Turnover and U t i l i z a t i o n . There i s l i t t l e doubt t h a t c h i c k s f e d excess l e v e l s o f Mn d e p o s i t t h i s m i n e r a l i n v a r i o u s body t i s s u e s . H a l p i n (24) i n v e s t i g a t e d the c a p a c i t y o f the c h i c k t o remove t h i s Mn from s t o r e d d e p o s i t s and t o use i t f o r normal b o d i l y f u n c t i o n s . Chicks were f e d e i t h e r 14 o r 2000 ppm Mn i n a c a s e i n - d e x t r o s e d i e t f o r two weeks (8 t o 22 days p o s t h a t c h i n g ) . A l l c h i c k s f e d 2000 ppm Mn were then switched t o 14 ppm Mn and s e r i a l l y k i l l e d on days 0, 3, 7, 10 and 14 f o l l o w i n g the d i e t s w i t c h . T i s s u e Mn c o n c e n t r a t i o n s are presented i n T a b l e I. D e p l e t i o n o f t i s s u e Mn was c u r v i l i n e a r with time. L o g - t r a n s f o r mation o f the d a t a , however, r e v e a l e d a l i n e a r (P
