Silicon_Bioavailability_Rats.pdf

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Silicon Bioavailability Studies in Young Rapidly Growing Rats

and Turkeys Fed Sernipurified Diets A Comparative Study

HENRY KAYONGO-MALE *'1 AND XIUJUAN J IA 2

'Departments of Biology and Microbiology and 2Chemistry and Biochemistry, South Dakota State University, Brookings,

South Dakota 57007-0595 Received January 10, 1998; Revised April 3, 1998;

Accepted April 15, 1998

ABSTRACT

Two experiments were conducted using completely randomized designs to study the bioavailability of Si from three sources to growing rats and turkeys fed semipurified diets. The basal diets were dextrose-egg albumin for rats and dextrose-casein for turkeys. The Si sources were tetraethylorthosilicate (TES), sodium silicate (NaSil), and sodium zeolite A (NaZA). Rats and turkeys were supplemented at 500 and 270 ppm Si, respectively, from each source. A control group of unsupplemented rats and turkeys was included in each experiment.

In general, irrespective of Si source, Si supplementation slowed (p < 0.05 or p < 0.01) growth rates in both rats and turkeys. Although dietary Si supplementation reduced (p < 0.05) plasma Mg levels and liver Zn concentrations in rats, it increased (p < 0.05) plasma P and reduced (p < 0.05) plasma Cu levels in turkeys.

Rats on TES had significantly slower (p < 0.05 or p < 0.01) growth rates (5-10~ than those on NaSil or NaZA. In rats, NaZA and TES reduced (p < 0.05) hemoglobin concentrations and plasma Zn, respectively. However, plasma Mg levels were higher (p < 0.05) in TES than NaSil- or NaZA-fed rats. The source of the dietary Si did not affect (p < 0.05) the organ weights of rats and their mineral concentrations.

Turkeys on TES diets grew at a significantly faster (p < 0.05) rate (15%) than those on NaSil or NaZA diets during the first 2 wk of experimentation. However, after 4 wk, there were no significant

*Author to whom all correspondence and reprint requests should be addressed.

Biological Trace Element Research ] 73 Vol 67, 1999

174 Kayongo-Male and Jia

(p > 0.05) differences in growth between the Si sources. In turkeys, NaZA increased (p < 0.05) hematocrit levels and plasma Mg levels. Turkeys on NaZA diets had larger (p < 0.05) hearts and livers than those on NaSil but not TES. Liver Mn content was higher (p < 0.05) in turkeys on NaSil than TES or NaZA. Heart Zn was lower (p < 0.05) in turkeys on NaSil than TES, but not NaZA.

Index Entries: Silicon, sodium silicate, sodium zeolite, tetraethylorthosilicate, tissue minerals, serum alkaline phosphatase.

INTRODUCTION

Silicon is the second most abundant element on earth (1). A large amount of silicon occurring in nature is in the form of aluminosilicates and polymeric silica and is, therefore, not biologically readily available (2). Ani- mal experiments have shown that the bioavailability of ingested silicon is very small and that the form of dietary silicon is an important factor deter- mining the rate of production of soluble or absorbable silicon from various silicon compounds in the gastrointestinal tract (3,4). Some forms of silicon in foods and beverages are readily absorbed from the gastrointestinal tract (2).

Tetraethylorthosilicate and sodium silicate have been reported to yield readily absorbable monosilicic acid in gastric stomachs with pH levels of less than 3.0 (5-7). Monosilicic acid is freely diffusible in tissue fluids (1,3). Sodium metasilicate, like tetraethylorthosilicate, has been used widely by researchers to study the biological functions of silicon (8,9). Sodium zeolite A containing about 15% silicon has been used as a silicon source by Wiegand et al. (10) to study silicon bioavailability in rats. Sodium zeolite A has a high silicon bioavailability (10). The draw- back with sodium zeolite A is that it also contains 13% aluminum, which may be toxic to some biological systems. Aluminum displaces magnesium and calcium from active sites of key enzymes, thereby inhibiting the cat- alytic action of those enzymes (11). Aluminum also disrupts calcium- dependent electrophysiological functions of muscles and may cause mortality from cardiovascular and respiratory dysfunctions (12).

The objective of this study was to compare the bioavailability of silicon from three sources: sodium silicate, tetraethylorthosilicate, and sodium zeolite A to young, rapidly growing rats and turkeys fed semipurified, dextrose-albumin- or dextrose-casein-based diets.

MATERIALS AND METHODS

Two experiments were conducted with young, rapidly growing rats and turkeys, using semipurified based diets. The basal diets were dextrose- egg albumin for rats and dextrose-casein for turkeys. The rapid growth phases of rats and turkeys are 8-12 and 4-6 wk of age, respectively. Three silicon compounds were used as sources of silicon (Si) to provide 270- and

Biological Trace Element Research Vol. 67, 1999

Silicon Bioavailability Studies 175

500-ppm Si levels of dietary inclusion for turkeys and rats, respectively. The three sources were (1) tetraethylorthosilicate or TES (J. T. Baker Chemical Co., Phillisburg, NJ) which is readily hydrolyzed in gastric stomach (pH < 3.0) to monosilicic acid that is available for absorption, (2) sodium silicate (Na2SiO3 �9 5H20) or NaSil (Matheson, Coleman and Bell, Norwood-Cincinnati, OH), and (3) sodium zeolite A or NaZA (Ethacal TM, Ethyl Corp., Baton Rouge, LA).

Experiment 1

Seventy-two (72) male Sprague-Dawley albino rats (SASCO, Omaha, NE) initially weighing, on average, 45.0 g were allotted into a four- dietary-treatment completely randomized experiment. The basal diet (Table 1) was a dextrose-egg-albumin type. In order to reduce avidin interference with biotin absorption, the spray-dried egg albumin was denatured by autoclaving at 120~ for 1 h and drying at 110~ for 1 h. The four dietary treatments included a control diet that inherently con- tained < 5.0 ppm Si, and three other diets supplemented with 500 ppm Si each obtained by additions of TES or NaSil or NaZA.

Animal care and management was similar to that described by Emerick and Kayongo-Male (13). Rats were weighed weekly during the 8-wk experimental period. At termination of the experiment, blood was drawn via heart puncture into heparinized vacuum tubes. Rats were killed by decapitation while under anesthesia. The heart, liver and femurs were collected from each rat and processed for chemical analyses as described by Emerick and Kayongo-Male (13).

Experiment 2 Seventy-two (72) newly hatched Nicholas tom turkey poults (Willmar

Poultry Co., Willmar, MN), weighing on average 54.3 g initially, were allotted into a four-dietary treatment, completely randomized experiment. The poults were caged in stainless-steel cages with elevated wire-mesh floors and were housed in the animal room having controlled temperature and lighting. The room temperature was kept at 35~ 32~ 29~ and 24~ during the first, second, third, and fourth week of the experiment, respectively.

The basal diet (Table 2) was a 28% protein, dextrose-casein type for- mulated to mimic the recommended nutrient content of the turkey starter diet (14). The four dietary treatments included a control diet (0 ppm Si) and three other diets supplemented with 270 ppm Si each, obtained by additions of TES or NaSil or NaZA.

The birds were weighed weekly during the 4-wk experimental period. At termination, a blood sample was drawn from each turkey via the V. provunda branchii wing vein into heparinized vacuum tubes. The birds were then killed by cervical dislocation followed by exsanguination. The heart, liver, and tibia were removed from each bird and processed for chemical analyses as described by Emerick and Kayongo-Male (13).


176 Kayongo-Male a n d Jia

Table 1 Rat Basal Diet Composition a

Ingredient Amount (%)

Dextrose, anhydrous 70.5

Egg albumin, spray dried 20.0

Salt mixture b 3.5

Vitamin mixture ~ 1.0

Corn oil 5.0

aDiet composition before the additions of the Si sources, as dietary variables.

bThe percentage composition of the salt mixture (AIN-76 salt mixture, ICN Biochemicals, Inc., Cleveland, OH, USA): calcium phosphate dibasic, 50.0; sodium chloride, 7.4; potassium citrate monohydrate, 22.0; potassium sulfate, 5.2; magnesium oxide, 2.4; manganous carbonate (43-48% Mn), 0.35; ferric citrate (16-17% Fe), 0.6; zinc carbonate, 0.66; cupric carbonate (53-55% Cu), 0.030; potassium iodate, 0.001; sodium selenite, 0.001; chromium potassium sulfate, 0.055.

cAIN-76 vitamin mixture (ICN Biomedicals, Inc) composition in grams/kilogram mixture triturated in dextrose: thiamine hydrochloride, 0.6; riboflavin, 0.6; pyridoxine hydrochloride, 0.7; nicotinic acid 3.0; D-calcium pantothenate, 1.6; folic acid, 0.2; D-biotin, 0.02; vitamin (cyanochobalamin) B12, 0.001; vitamin A (retinyl palmitate, 250,000 IU/g), 1.6; vitamin E (DL-alpha-tocopherol acetate, 250 IU/g), 20; vitamin D3 (cholecalciferol, 0.25; vitamin K (medaquinone), 0.005.

General Procedures

In both experiments, a 12-h day-and-night cycle was maintained. An attempt was made to minimize silica contamination by initially cleaning the animal room and related equipment followed by a weekly flushing of the painted concrete floor. Every day, the birds and rats were given ad libitum access to fresh diets and distilled water provided in stainless- steel feeders and water containers.

Chemical A n a l y s e s

Determinat ion of hematocri t and hemoglobin were done immedi- ately following the collection of the blood samples using s tandard procedures described by Emerick and Kayongo-Male (13). Plasma separated from hepar inized blood samples and stored at -25~ was used for cholesterol, enzyme, and mineral assays. Plasma total cholesterol was de termined using enzymatic kits (Sigma kit 352-50, Sigma Chemical Co., St. Louis, MO). Serum alkaline phosphatase activity was determined by the hydrolysis of p-nitrophenyl phosphate (Sigma kit 104, Sigma Chemical Co., St. Louis, MO).


Silicon Bioavailability Studies

Table 2 Turkey Basal Diet Composition a

177

Ingredient Amount (%)

Dextrose, anhydrous 51.2

Casein 33.0

Solka flock 3.0

Corn oil 4.0

L-Arginine 0.4

DL-Methionine 0.4

Mineral mixture ~ 7.0

Vitamin mixture ~ 1.0

aDiet composition before the additions of the Si sources, as dietary variables.

bMineral mixture composition in grams/kilogram triturated in finely powdered sucrose: calcium diphosphate, dibasic, 313; calcium carbonate, 197; sodium chloride, 72.6; potassium chloride, 21.0; potassium citrate, monohydrate, 246; magnesium sulfate, anhydrous, 42.4; manganous carbonate, 1.8; ferric citrate, 6.71; zinc carbonate; 1.92; cupric carbonate, 0.024; chromium potassium sulfate. 12H20, 0.22; tin sulfate, 0.09; potassium iodate, 0.01; sodium selenite, 0.01.

cVitamin mixture composition in grams/kilogram triturated in finely powdered sucrose: vitamin A palmitate (500,000 IU/g), 1.0; vitamin D3 (400,000 IU/g), 0.30; vitamin E acetate (500 IU/g), 4.0; menadione sodium bisulfite, 3.0; choline bitartrate, 211; thiamine HC1, 0.22; riboflavin, 0A; pyridoxine HC1, 0.55; niacin, 6.00; calcium pantothenate, 1.10; folic acid 0.1; biotin, 0.03; vitamin B12 (0.1%), 1.0.

Calcium (Ca), magnesium (Mg), and zinc (Zn) in plasma plus copper (Cu) and Zn in nitric acid digests of liver and heart tissues were determined by flame atomic absorption spectrophotometry (Perkin- Elmer Model 5100PC, Norwalk, CT) as described by Stewart et al. (15). Phosphorus (P) in plasma was determined using the Fiske and Subbarow phosphomolybdate method (16). Plasma Cu was assayed by graphite fur- nace atomic absorption (Model 5000 equipped with Model 500 heated graphite atomizer and autosampler, Perkin-Elmer) using 0.2% nitric acid (Utrex, J. T. Baker Chemical) as diluent.

Statistical analysis of the data was done by the general linear model (GLM) analysis of variance (ANOVA) procedures using a model con- sisting of four dietary treatments based on a Si source for the two experiments (17). The Fisher-protected least square difference (LSD) test



was used to identify significant differences among treatment means. Standard errors of the means were calculated from the error mean squares (18).

RESULTS

Growth Data

Rats The rat growth data are shown in Fig. 1. The addition of dietary Si

from the different sources significantly affected (p < 0.05 or p < 0.01) rat body-weight changes. From the third to the fifth week of Si supplementation, the rats on TES had a significantly slower (p < 0.05) growth rate than those on NaSil but not NaZA. During the sixth week, the rats on TES had a significantly slower (p < 0.05) growth rate than those on NaZA but not NaSil. During the seventh and eighth week, rats on TES had a significantly slower (p < 0.05) growth rate than those on NaSil or NaZA. After 8 wk of Si supplementation, rats on TES, NaSil and NaZA weighed, on average, 235, 257, and 268 g, respectively. At the same time, the weight of the rats on the control diet was 273 g, which was significantly higher (p < 0.05) than that of rats on the TES but not on the NaSil or NaZA diets.

Turkeys The turkey growth data are shown in Fig. 2. Dietary supplemental Si

from different sources significantly affected (p < 0.05 or P < 0.01) turkey growth. During the first week of silicon supplementation, the turkeys on NaSil diet had a slower (p < 0.05) growth rate than turkeys on the control and TES diets but not those on the NaZA diet. During the second week, the control and TES turkeys grew faster (p < 0.05) than turkeys on NaSil or NaZA. However, in the third week, turkeys on the control diet grew faster (p < 0.05) than those on NaSil or NaZA diets but not those on TES diets. Within the Si-supplemented groups, turkeys on TES diets grew faster (p < 0.05) than those on NaSil or NaZA diets during the second week but not during the third week of the experiment. After 4 wk of Si supplementation, there were no significant differences (p > 0.05) in the growth rates of all turkeys on the four dietary treatments although the unsupplemented turkeys weighed more than the Si-supplemented turkeys (834 vs 760 g).

Blood Data

Rats The rat blood data are presented in Table 3. Hemoglobin content was

significantly affected (p < 0.05) by Si source. Rats on the NaZA diet had lower (p < 0.05) hemoglobin levels than rats on the rest of the diets. Plasma Ca, Mg, and Zn were significantly affected (p < 0.05) by Si source but not plasma Cu and P. Plasma Ca content was lower (p < 0.05) in rats



Fig. 1. Body-weight changes of rats fed diets containing silicon from various sources during the 8-wk experimental period. Silicon sources: Cont = control with no silicon added; NaSil = sodium silicate (Na2SiO3.5H20); TES = tetraethylorthosilicate; NaZA = sodium zeolite A (15% silicon); SEM = standard error of the mean calculated from the error mean squares; a, b, c = graph columns, within 1 wk on the experiment, not sharing a common letter(s) differ at p < 0.05.

on NaSil diet than the control diet bu t not the TES or N a Z A diets. Plasma Mg levels were h igher (p < 0.05) in the control rats than the Si supple- m e n t e d rats. Within the Si s u p p l e m e n t e d rats, rats on the TES diet had h igher (p < 0.05) Mg levels than those on NaSil or N a Z A diets. Rats on TES diets had lower (p < 0.05) p lasma Zn levels than those on the control and N a Z A diets bu t not NaSil diets.

Turkeys The tu rkey blood data are s h o w n in Table 4. Hematocr i t levels and

not hemoglob in content were significantly affected (p < 0.05) by the Si



Fig. 2. Body-weight changes of turkeys fed diets containing silicon from various sources during the 4-wk experimental period. Silicon sources: Cont = control with no silicon added; NaSil = sodium silicate (Na2SiO3.5H20); TES = tetraethylorthosilicate; NaZA = sodium zeolite A (15% silicon); SEM -- standard error of the mean calculated from the error mean squares; a, b, c = graph columns, within I wk on the experiment, not sharing a common letter(s) differ at p < 0.05.

source. Turkeys on the NaZA diet had higher (p < 0.05) hematocri t levels than turkeys on the control diet but not those on the NaSil or NaZA diets. Plasma P, Mg, and Cu were significantly affected (p < 0.05) by the Si source but not p lasma Ca and Zn. Turkeys on the control diet had lower (p < 0.05) p lasma P levels than the s u p p l e m e n t e d turkeys whose P levels were not different (p > 0.05) be tween the Si sources. Plasma Mg levels were higher (p < 0.05) in the turkeys on the NaZA diet than the tu rkeys on the control and NaSil diets bu t not TES diet. Turkeys on the control diet ha d h igher (p < 0.05) p l a sma Cu levels than the Si- supp l emen ted turkeys whose Cu levels were not different (p > 0.05)



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Silicon Bioavailability Studies

Table 5 Mineral Concentrations and Weights

183

Mineral Concentrations Weights ~

Dietary Treatment Heart Liver Heart Liver

Copper Zinc Copper Zinc

. . . . . . . . . . ppm, dry basis . . . . . . . . . . . . . . . % . . . . . .

Control 23.3 79.7 12.8 95.2 a 0.33 3.67

TES 23.2 78.7 12.5 89.1 b 0.37 3.96

NaSil 22.1 76.0 11.7 88.5 b 0.35 3.74

NaZA 21.6 77.4 11.5 88.9 b 0.33 3.66

SEM 2 1.11 1.94 0.44 1.76 0.01 0.10

GLM 3 NS NS NS .025 NS NS

1Heart and liver weights expressed as percent of final (8th week) 'bodyweight ' Standard error of the mean calculated from the error mean square. A one-way analysis of variance using Type III sum of squares; numerical values are

levels of probability; NS = not significant (p > 0.05) Least square means within a column not sharing a common superscript letter differ

at p < 0.05.

between the Si sources. Total plasma cholesterol and serum alkaline phosphatase activity were not affected (p > 0.05) by the Si source.

Organ Data Rats

The rat liver and heart weights and their mineral concentrations are shown in Table 5. The source of Si did not affect (p > 0.05) organ weights or their mineral concentrations except liver Zn concentrations. Liver Zn concentrations were higher (p < 0.05) in the unsupplemented than the Si- supplemented rats. Within the Si-supplemented groups, liver Zn levels did not significantly (p > 0.05) differ.

Turkeys The turkey liver and heart weights and their mineral concentrations

are shown in Table 6. The source of Si significantly (p < 0.05) affected heart and liver weights and liver Mn and heart Zn concentrations. Tur- keys on NaZA diets had larger (p < 0.05) hearts and livers than turkeys on the control and NaSil diets but not those on the TES diets. Turkeys supplemented with NaSil had the smallest hearts and livers. Liver Mn content was higher (p < 0.05) in turkeys on NaSil than TES and NaZA diets but not the control birds. Heart Zn was lower (p < 0.05) in turkeys on the control and NaSil than TES diets but not the NaZA diets.


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DISCUSSION

The NaSil- and NaZA-supplemented diets supported growth much better than TES in rats. The differences in growth rates of rats among the three silicon sources persisted throughout the entire 8 wk of study. How- ever, in turkeys, the TES promoted growth much better than NaSil and NaZA. The finding, in rats, that NaZA and NaSil diets supported supe- rior growth performance, is consistent with previous reports. In studies involving biological functions of Si, Weigand et al. (10) and Najda et al. (8) showed higher Si bioavailability from NaZa and NaSil, respectively. NaZA lowered hemoglobin content in rats. This reduction might be related more to its A1 content than its Si availability. NaZA contains about 13% A1. Aluminum has been shown to bind to transferrin and inhibit Fe transportation by this protein (19). This interference could have caused a reduction in Fe available for hemoglobin synthesis and, therefore, a drop in hemoglobin values.

The NaZA supplementation of turkeys increased plasma Mg levels, which supports the report by Birchall (11) that A1 displaces Mg from tissues and key enzymes, hence the increase in circulating plasma Mg levels. The NaZA-supplemented turkeys had also significantly enlarged hearts and livers compared to NaSil supplementation but not TES. This could again be due to the antagonistic effects of the NaZA-inherent A1 to Fe and Cu, creating anemic and hypocupric conditions. Hypocupria has been associated with cardiac hypertrophy (20,21). It should be pointed out that although the hepatic and cardiac tissue Cu concentrations were generally lower for NaZA diets than NaSil and TES, this reduction was not significantly different. In turkeys, NaZA supplementation significantly reduced liver Mn levels compared to NaSil but not TES. Carlisle (4) reported that Si depressed Mn bioavailability. In case of NaZA the antagonistic interaction between Si and Mn could also have been augmented by the antagonistic effects of the NaZA-inherent A1 on Mn, a bivalent cation. Birchall (11) reported that A1 displaced bivalent cations like Ca and Mg. A number of turkeys in this treatment group seemed to show early symptoms of perosis, a Mn-deficiency dis- ease in birds (22).

Where rats and turkeys responded to the Si sources differently could be due to the differences in the anatomical structure of the gastrointestinal tracts of the two species. This definitely affects the location and extent of hydrolysis or solubility of the various compounds and, therefore, Si absorption. It could also be due to the fact that NaSil and NaZA are inorganic compounds, whereas TES is an organic com- pound and, therefore, probably handled differently by the two species. It should also be pointed that slight variations in total Si intake by the species might account for some of the observed differences too.



CONCLUSION

Rats and turkeys fed NaZA diets performed better than those on NaSil or TES diets. Although NaZA was most effective in promoting higher growth rates, it also had negative side effects on hemoglobin content, heart and liver weights, and hepatic Mn concentrations. These side-effects were deemed to be due to the 13% inherent A1 content of NaZA. Aluminum may have interfered with the metabolism of other trace elements, such as Fe, Cu, and Mn. Such negative side effects could have disastrous effects on animal health when supplemented with NaZA over long periods of time.

ACKNOWLEDGMENTS

We are grateful for the help of Dr. R. J. Emerick and Dr. I. S. Palmer, the technical support of Renata Wnuk and Nancy Anderson, and the skillful preparation of the manuscript by Vickie Molengraaf.

This work was funded by the USDA Contract #9404222.

REFERENCES

1. R. K. Iler, The Chemistry of Silica, Wiley, New York, (1979). 2. C. D. Seaborn and F. H. Nielsen, Nutr. Today 28, 13-18 (1993). 3. E. M. Carlisle, Silicon in Trace Elements in Man and Animal Nutrition, Vol. 2, 5th ed.,

W. Mertz, ed., Academic, New York, pp. 373-390 (1986). 4. E. M. Carlisle, Ciiba Found. Symp. 121, 123-139 (1986). 5. E. M. Carlisle, Science 178, 619-621 (1972). 6. R. J. Emerick, Nutr. Rep. Int. 34, 907-913 (1986). 7. R. J. Emerick, J. Nutr. 117, 1924-1928 (1987). 8. J. Najda, J. Gminski, M. Drozdz, and A. Danch, Biol. Trace Element Res. 37, 107-114 (1993). 9. K. Schwarz and D. B. Milne, Nature 239, 333-334 (1972).

10. K. E. Wiegand, Poultry Sci., 70, (Suppl.1), 131 (1991). 11. J. D. Birchall, Silicon and the bioavailability of aluminum--nutritional aspects, in

Food, Nutrition and Chemical Toxicity, D. V. Parke, C. Ioannides, and R. Walker, eds., Smith-Gordon, Great Britain, pp. 215-226 (1993).

12. T. P. A. Kruch and D. R. Mclachlan, Mechanisms of aluminum neurotoxity relevance to human diseases, in Metal Ions in Biological Systems, Vol. 24, H. Sigel and A. Sigel eds., Marcel Dekker, New York (1988).

13. R. J. Emerick, and H. Kayongo-Male, J. Nutr. Biochem. 1, 35-40 (1990). 14. National Research Council, Nutrient Requirements of Poultry, 9th ed., National Academy

Press, Washington, DC (1994). 15. S. R. Stewart, R. J. Emerick, and H. Kayongo-Male, J. Anim. Sci. 71, 946-954 (1993). 16. B. L. Oser, Hawk's Physiological Chemistry, 14th ed., McGraw-Hill, New York (1965). 17. SAS, SAS Procedures Guide (Release 6.03 Ed.), SAS Institute Inc., Cary, NC (1988). 18. R. G. D. Steel and J. H. Torrie, Principles and Procedures of Statistics: A Biomedical

Approach, 2nd ed., McGraw-Hill, New York (1980). 19. A. C. Alfrey, Aluminum, in Trace Elements in Human and Animal Nutrition, Vol. 2, 5th

ed., W. Mertz, ed., Academic, New York, pp. 399-413 (1986). 20. L. M. Klevy, Ann. NY Acad. Sci. 355, 140-151 (1980). 21. L. M. Klevy, Clin. Geriatr. Med. 3, 361-372 (1987). 22. L. S. Hurley, and C. L. Keen, Manganese, in Trace Elements in Human and Animal

Nutrition, Vol. 1, 5th ed., W. Mertz, ed., Academic, New York, Vol. 1, pp. 185-224 (1987).


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