Interactions of Cadmium with Copper, Iron, Zinc, and Manganese in Ovine Tissues1 JOHN J. DOYLE 2 AND WILLIAM H. PFANDER Animal Science Research Center, University of Missouri, Columbia, Missouri 65201 ABSTRACT Diets containing 0, 5, 15, 30, and 60 ppm of cadmium were fed to male lambs for 191 days to ascertain what effect cadmium might have on the tissue concentrations of copper, zinc, iron, and manganese. The cadmium content of all tissues increased with an increase in dietary cadmium. The iron concentration of the ileum tissue was significantly depressed in the cadmium-treated groups compared with that of the controls. Liver copper, iron, and manganese were significantly depressed and liver zinc significantly increased by varying levels of dietary cadmium. The copper concen trations of the spleen and testicles were significantly decreased by all levels of cadmium while the copper and zinc concentrations of the kidneys were significantly increased in the 30 and 60 /¿gCd/g and 15, 30, and 60 /¿gCd/g groups, respectively. In general, cadmium had no significant effect on the rumen, abomasal, heart, or lung concentrations of copper, zinc, iron, or manganese. J. Nutr. 105: 599-606. 1975. INDEXING KEY WORDS manganese •tissues

cadmium •lambs

interactions

The toxic effects of cadmium on specific biochemical and physiological parameters in animals are well known (1-8). Trace metals such as zinc, selenium, iron, copper, and cobalt, and certain nonmetals have been shown to overcome these effects in part or in toto (9-15). Furthermore, zinc and selenium have protective effects against the carcinogenic, teratogenic, and hypertensinogenic3 effects of cadmium ( 16-19 ). Cadmium interactions with other trace metals in the tissues of several species have been studied extensively. It was shown that the zinc concentration of many tissues is increased by dietary cadmium (4, 6, 9, 10, 20-23). In addition, other researchers have reported that tissue concentrations of iron, copper, and manganese * are lowered by relatively high levels of dietary cadmium (9,10,20,24-26). In relation to cadmium interactions with macroelements, Vander (27) reported de creased urinary sodium and potassium ex cretions in dogs injected with CdCl2, whereas Lener and Musil (28) found de creased urinary sodium excretion in rats fed dietary cadmium. Doyle et al. (29) re 590

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copper

zinc

iron

ported increased retention of 24Na in rats fed low levels of cadmium. Kobayashi ( 30 ) showed that the feeding of a calciumdeficient diet plus cadmium to rats caused a significant loss of calcium from the bone. Itokawa et al. (31) showed that mag nesium levels in bone were decreased, and calcium levels in muscle increased in rats fed a cadmium-supplemented, low protein, calcium-deficient diet. The data presented in this report show the effects of various levels of dietary cad mium on some trace-element concentra tions in various organs and tissues of male lambs fed for 191 days a diet supplying 2,630 kcal digestible energy and 93 g di gestible protein/kg and adequate amounts of other nutrients known to be required by sheep. Furthermore, we were interested in Received for publication November 12, 1974. 1Journal Series no. 1704. Approved by the Director of the Missouri Agricultural Experiment Station. "Current address: Human Nutrition Laboratory, DSDA, 2420-2nd Avenue North, P.O. Box D, Univer sity Station, Grand Forks, N.D. 58201. 3Perry, H. M. & Erlanger, M. W. (1974) Pre vention of cadmium-Induced hypertension by selenium. Federation Proc. 33, 357. (Abstr.) •Fox.M. K. S.. Jacobs, R. M. & Fry, B. J. (1971) Protection against cadmium by iron and ascorbic acid. Federation Proc. 30, 238. (Abstr.)

coo

JOHN J. DOYLE AND WILLIAM H. PFANDER TABLE 1

overNo.Treatment CdControl5

191-day period1-*Cu9.0

dietary cadmium

animals

0.21°0.50 ± 6.0°53.1 ± 0.04°1.60 ± 6.8°48.6 ± Cd15 „g/g 0.52°*2.30 ± 6.3°42.2 ± Cd30 „g/g 0.18*3.61 ± 3.6°38.6 ± Cd60 „g/g ±0.67'Fe48.3 ±3.2«a „g/gCd6666ti0.44 1 Data are means ±SEM.

0.6°11.8 ± 5.5°135.1 ± 2.8°43.8 ± 2.2°10.2 ± 35.2"101.5 ± 8.6*43.3 ± 0.6°10.2 ± 3.9°103.0 ± 11.0*19.2 ± 0.9°9.1 ± 3.2°105.0 ± 4.7°22.8 ± ±0.7°Zn85.9 ± 2.8°Ma15.6 ± 3.5«'

» Data with different superscripts are significantly different (P < 0.05).

the accumulation of cadmium in such ed ible tissues as liver, kidney, and heart. MATERIALS AND METHODS

The experimental animals were pre viously described by Doyle et al. (8). Briefly, 30 male lambs, approximately 4 months old, were allotted by weight into five lots of six and fed ad libitum diets for 191 days. The diets contained 0, 5, 15, 30, and 60 ¿¿g/g of added cadmium. After the experimental period of 191 days, all animals were killed, and total liver, kidneys, testicles, spleen, and heart were collected and freeze-dried for future analyses. Body and organ weights of the animals have been previously reported (8). Samples from the apex of both lungs, the proximal ileum, the anterior ventral rumen, and the fundus of the abomasum were also collected and freeze-dried for future analyses. All organs and tissues were washed in running tap water before freez ing and were ground through a Wiley mill5 equipped with a 2-mm sieve after freeze-drying. Cadmium, copper, iron, zinc, and manganese concentrations of all organs

and tissues collected were determined by atomic absorption °using the boat method for low concentrations.7 Digestion was by the nitric acid-perchloric acid method (32). The deuterium background corrector was used in the determination of cadmium andAnalysis zinc. of variance and Duncan's New Multiple Range Test were used to ascer tain differences among treatments (33). RESULTS AND DISCUSSION

The cadmium concentration in all tissues increased with increasing levels of cad mium in the diet (tables 1-9). The same trend has been reported by other investi gators using other species (4, 6). Although the concentration of cadmium was greater in the kidneys than in the liver (tables 4 and 9) for all treatments, the total cad mium was greater in the liver (8). Con centrations of cadmium were low in spleen, * Model #3,

Arthur

H. Thomas Co., Philadelphia,

Pa. .

• Perkln-Elmer, model 403 spectrophotometer. ' Kahr, H. L., Peterson, G. B. & Schallls, J. P. (1908) Atomic micro sampling the "sampling hont" absorption technique. Atomic AbsorptionwithNew»letter, 7, 35.

TABLE 2 Concentrations of cadmium, iron, copper, zinc, and manganese in dry abomasal tissue of lambs fed dietary cadmium over a 191-day period1-1 TreatmentControl5 animals46553Cd1.6

Cd15 „g/g

Cd30 „g/g Cd60 „g/g „g/gCdNo. 1 Data are means± SEM.

M51.5

1.4°8.1 ± 0.5«1.3 ± ±11.3°61.8 0.2°2.8 ± 5.2«70.8 ± 0.7°10.5 ± 0.4°5.4 ± 2.0°64.7 db 2.1«9.9 ± 0.9*10.6 ± 1.1°7.5 ± 5.9°53.2 ± ±1.6*Fe73.0 ± 2.7«CuM/a9.1 ±0.4«Z Data with different superscripts are significantly

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6.2«50.5 ± 0.3»3.5 ± 7.6°49.5 ± 0.3«3.7 ± 0.3°3.3 ± 3.9°53.8 ± 5.4«49.3 ± 0.3«3.2 ± ±5.8«Mn4.0±0.1«

different (P < 0.05).

CADMIUM

001

IN OVINE TISSUES

TABLE 3 Concentrations of cadmium, iron, copper, zinc, and manganese in dry ilcum tissue of lambs fed dietary cadmium over a 191-day period1* Treatment

No. animals

Mn

Cu

Control5 Cd15 „g/g Cd30 „g/g Cd60 „g/g „g/gCd666661.11

0.22"2.24 ± 0.75«4.26 ± 1.38«7.19 ± 2.22°19.02 ± ±6.686129.9

20.2«91.0 ± 0.3°9.3 ± 3.3°85.7 ± 0.7«3.6 ± 14.3"85.9 ± 0.7°9.2 ± 4.4«78.7 ± 0.9°3.5 ± 12.0"81.2 ± 1.0°3.2 ± 0.5«9.7 ± 0.9«81. ± 7.5»76.0 ± 0.6°3.4 ± 0.5°8.8 ± ±4.4«82.7 7 ±0.7° ± 8.0"M/a10.3 ±0.3°79.1 ±2.5«5.1

1 Data are means • SEM.

' Data with different superscripts are significantly different (P < 0.05).

lung, testicles (tables 6-8), rumen, abomasal, and small intestinal tissues (tables 1-3 ) ; concentrations were least in the heart (table 5). A comparison of the control tis sues with the tissues of lambs fed 60 /xg/g in their diet showed an increase of from 7-fold (abomasum) to 238-fold (liver) after cadmium supplementation. The ef fects of the added cadmium on the content of the other minerals are presented in the tables in the order that the cadmium would be encountered. There are marked differ ences in the magnitude of response of the tissues studied to the 60 ppm added cad mium. Abomasal and heart, which in creased in cadmium concentration by 7and 44-fold, respectively, had no significant changes in their concentration of minerals. Testicles, lungs, and spleen, which had cadmium increases of 45, 64, and 93, re spectively, had decreased copper concen trations. Rumen tissue. There were no significant differences ( P < 0.05 ) in the iron, copper, or zinc concentrations of rumen tissue (table 1). However, distinct downward and upward trends appeared in the con

centrations of iron and zinc, respectively, with increases in dietary cadmium. There was an increase in manganese at lower levels of cadmium. Abomasal tissue. Cadmium did not have a significant effect on the iron, copper, zinc, or manganese concentrations of abomasal tissue (table 2). The 60 /¿g/gdietary cad mium appeared to depress the levels of iron, copper, and manganese relative to the levels of the controls. lieu m tissue. The trace-element compo sition of the ileum is shown in table 3. The concentration of iron was significantly greater in the controls than it was in the cadmium-supplemented groups. Fox et al.4 showed that excess dietary cadmium caused decreased levels of iron in the small intestinal mucosa of Japanese quail and suggested that the increased cadmium lev els of the small intestine interfered with the absorption of required minerals. Cop per and manganese levels were slightly but not significantly decreased in the 60 /u.g Cd/g group compared with those of the controls, whereas zinc levels varied little between treatments.

TABLE 4 Concentrations of cadmium, iron, copper, zinc, and manganese in dry liver of lambs fed dietary cadmium over a 191-day period1'* Treatment

No. animala

Cd

Cu

Zn

0.26«14.92 ± 27.5°212.1 ± 74.0°318.4 ± 10.2°140.9 ± Control5 1.51"*51.72± ± ±20.1*325.8 39.3»363.1 ± 9.0«166.6 ± Cd15 „g/g 4.17°*62.73 47.5«204.7 ± 54.4'289.5 ± 4.1«'188.1 ± Cd30 „g/g 3.13*275.94 ± 12.1"179.5 ± 52.6*193.5 ± 7.7*208.2 ± Cd60 „g/g db 38.69"369.4 ±IS.S6M/O687.9 ±62.7»125.0 ±16.8612.3 „g/gCd666661.69 1 Data are means ±SEM.

>Data with different superscripts are significantly different.

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Mn

0.9«12.5 ± 0.3°13.3 ± 0.7«11.9 =b 0.3«9.4 ± ±0.5"

002

JOHN J. DOYLE AND WILLIAM H. PFANDER TABLE 5 Concentrations of cadmium, iron, copper, zinc, and manganese in dry heart of lambs fed dietary cadmium over a 191-day period1•*

Treatment

No. animala

Cd

Cu

Fe

Zn

Mn

0.01°0.24 ± 3.77°164.09 ± 0.79°14.30 ± 2.19°69.49 ± 0.12«1.49 ± Control5 0.03°0.43 ± 3.49°164.78 ± 0.76°13.81 ± 2.78°72.12 ± 0.11°3.38 ± Cd15 Mg/g 0.08°1.28 ± 8.00°205.64 ± 0.77°13.22 ± 7.52°63.82 ± 1.74«1.58 ± Cd30 Mg/g 0.12"2.66 ± 19.36°176.22 ± 0.36°13.30 ± 2.93«69.63 ± 0.36°1.49 ± Cd60 Mg/g ±0.58k167.64 ±20.39«M/a14.83±0.63«69.83 ±3.26°1.78 ±0.12« Mg/gCd66(i660.06 1 Data are means ±SEM.

* Data with different superscripts are significantly different (P < 0.05).

Liver. The iron concentration of the liver was significantly greater in the controls than in the 30 and 60 /*g Cd/g groups (table 4). This is consistent with the find ings of Bunn and Matrone (9), Banis et al. (10), Fox and Fry (11), Whanger (26), and Hennig et al. (34). However, Anke et al. (20) reported a highly significant (P < 0.001 ) increase in the liver iron concentra tion of hens fed 200 /tg/g of dietary cad mium for 28 days. These authors concluded that the loss of iron from the muscles, bones, and feathers, due to the dietary cad mium, accumulated in the liver with a con sequent increase in liver iron concentration. The copper concentration of the liver was significantly greater in the controls than in all other groups (table 4). Bunn and Matrone (9), Fox and Fry (11), Anke et al. (20, 24), Mills and Dalgarno (25), and Campbell and Mills 8 reported similar results for rats, Japanese quail, goats, sheep, and rats, respectively. Anke et al. ( 20, 24 ) reported significantly higher levels of copper in the livers of hens fed 200 ju.g Cd/g of diet for 28 days than in the livers of controls, whereas Schroeder and Nason (23) found higher levels in the livers of

rats fed 50 /¿gCd/ml of drinking water for approximately 30 months than in the livers of controls. Dietary cadmium significantly increased the zinc concentration in the livers of the 30 and 60 /tg Cd/g groups compared with those of the controls. This result agrees with data reported by Powell et al. (4) in calves, Bunn and Matrone (9) in rats, Schroeder and Nason (23) in rats, and Anke et al. (24) in goats, bulls, rabbits, ducks, and hens. However, Mills and Dal garno (25) showed that the zinc concen tration in lamb liver was significantly de pressed by low levels of dietary cadmium. The manganese concentration of the liver was significantly decreased in the 60 ¿ig Cd/g group relative to that of the controls. Fox et al.4 reported a similar result with Japanese quail. Schroeder and Nason (23) showed that high levels of cadmium in the drinking water of rats significantly in creased the manganese concentrations of the liver relative to the controls. It is not clear why such differences should occur as »Campbell, J. K. & Mills, C. F. (1973) Effects of dietary cadmium and zinc on rats maintained on diets low In copper. Proc. Nutr. Soc. 33, ISA.

TABLE 6 Concentrations of cadmium, iron, copper, zinc, and manganese in dry spleen of lambs fed dietary cadmium over a 191-day period1•* Treatment

No. animals

rd

Fe

Cu

Zn

.Mn

1.59°7.98 ± 7.17«113.21 ± ±0.17«1.67 0.02«0.36 db ±511.04±628.78 Control5 1.13»7.72 ± 2.95°105.98 ± 0.23°1.16 ± 0.03°2.15 ± Cd15 Mg/g 3.80°108.58 ± 0.08«1.52 ± 0.79»6.90 ± 0.17«7.14 ± ±475.65 Cd30 Mg/g 4.09°106.93 ± 0.32«4.00 ± 0.24»8.22 ± 0.49»13.34 ± ±2,115.51 Cd60 Mg/g ±0.14»113.78 ±6.24°1.10 ±2.86« Mg/gCd66(i660.14 ±1.70»959.42 ±168.0°63.90«87.30«59.10°1,206.00«12.70 ' Data are means ±SEM.

*Data with different superscript«are significantly different (P < O.OS).

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CADMIUM IN OVINE TISSUES

603

TABLE 7 Concentrations of cadmium, iron, copper, zinc, and manganese in dry lungs of lambs fed dietary cadmium over a 191-day period*-2 No. animals

CdControl Treatment

5 „g/gCd 15 „g/gCd 30 Mg/g Cd 60 „g/gCdfi

0.72 (i 1.63 6 4.34 6 60.138.32

1 Data are means

• SEM.

±0.03« ±0.00« ' 516.18 ±0.17* 329.01 ±0.25e 523.60 ±0.99°Fe818.23 504.20

±0.64°* ±9.43° ±0.16° ±438.00« ± 60.40° 16.74 ±0.46° 82.38 ±1.14° 1.58 ±0.29° 77.18 ±4.41° 1.85 ±0.30° ± 43.70° 9.91 ±0.36* ±258.00° 10.09 ±0.49°' 79.58 ±4.41° 2.07 ±0.74° 1.96 ±0.54° ±145.00°Cumia12.51 11.58 ±0.57°*Zn83.38 75.62 ±3.08°Mn2.96

* Data with different superscripts are significantly different (P < 0.05).

the concentrations of the metal fed by the different investigators were similar. Heart. The trace-element composition of the heart is shown in table 5. The concen trations of iron, copper, zinc, or manganese did not vary greatly among treatments. Cousins et al. (6) reported similar zinc results in swine. In contrast, Schroeder and Nason (23) found that the concentration of zinc in the hearts of rats given cadmium in their drinking water over an extended period of time was significantly ( P < 0.005) elevated over that of the controls. The copper and manganese levels in the heart were similar to data reported by Schroeder and Nason (23) for rats. Spleen. The copper concentration of the spleen in the treated groups was signifi cantly lower than that in the controls (table 6). Schroeder and Nason (23) re ported no significant differences in traceelement content of spleen between rats supplied 50 /xg Cd/ml in their drinking water and controls over a period of ap proximately 30 months. The iron value for spleen in the 60 /¿gCd/g is extremely high due to one animal. Hence, it is possible that the high iron value and large variation

might be due to residual blood in the spleen of this animal. Lungs. There were no significant differ ences in the iron, zinc, or manganese con centrations of the lungs between treatments (table 7). However, there appeared to be a trend in decreased concentrations of these elements with increased dietary cad mium. Cousins et al. (6) reported similar zinc results in swine. However, in contrast, Schroeder and Nason (23) found that the zinc concentration in lungs of rats fed di etary cadmium for 30 months was signifi cantly greater than that in the controls. Testes. The testicular copper concentra tion was significantly greater in the con trols than in the other treatments ( table 8 ). The iron concentration was slightly but not significantly lower in the 15, 30, and 60 fig Cd/g groups than it was in the con trols. Banis et al. (10) reported similar results for rats, but found that excess di etary iron increased the iron content of the testes to near normal levels. It is highly probable that the decrease in iron and copper concentrations of the testes is, in part, a reflection of the decrease in the

TABLE 8 Concentrations of cadmium, iron, copper, zinc, and manganese in dry testicles of lambs fed dietary cadmium over a 191-day period1•* animalsControl5 Treatment

No.

0.02°0.43 ± 4.70°85.47 ± 21.70«126.80 ± 0.59°6.52 ± 0.10«2.44 ± 0.53°1.15 ± 22.50«92.79 ± 0.19*6.81 ± 1.92«84.69 ± 0.04«2.28 ± Cd15 „g/g 0.19°2.87 ± 5.26«93.97 ± 0.14*6.43 ± 5.88°79.34 ± 0.06°2.54 ± Cd30 „g/g 0.14»5.43 ± 0.24»6.67 ± 2.88°89.32 ± 1.90°74.82 ± 0.07«2.20 ± Cd60 „g/g ±0.33*Zn76.64 ±6.00«Mn2.21±0.12« „g/gCd6666fiCd0.12 ±1.046Fé121.39± 7.75«Cuvali7.81 1Data are means ±BEH.

• Data with different superscripts are significantly different (P < 0.05).

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604

JOHN J. DOYLE AND WILLIAM H. PFANDER TABLE 9 Concentrations of cadmium, iron, copper, zinc, and manganese in dry kidneys of lambs fed dietary cadmium over a 191-day period'-*

Treatment

No. animals

Cd

Fe

Cu

Mn

0.50»58.85 ± 504.7«307.9 ± 0.5°18.6 ± 4.4°149.9 ± 0.3»6.0 ± Control5 3.50°187.62 ± 83.4°501. ± 2.1°»17.6 ± 5.9°*209.2 ± 0.3°5.6 ± Cd15 Mg/g 19.50»426.81 ± ±250.0«281.7 3 0.4°»18.8 ± 8.4»254.9 ± 0.2°5.8 ± Cd30 Mg/g 30.30'768.84 ± 60.7°714.5 ± 0.6»20.0 ± 24.2»250.9 ± 0.1°5.3 ± Cd60 Mg/g ±83.30*892.8 ±564.2«m/o14.9±1.2*111.8 ± 8.6»5.3 ±0.2° „g/gCd66B664.42 1 Data are means ±SEM.

* Data with different superscripts are significantly different (P < 0.05).

blood supply to the testes, which is a direct action of cadmium (35). There were no significant differences among treatments in the zinc concentration of the testes. Similar results have also been reported by Powell et al. (4) in calves and by Banis et al. (10) in rats. Bunn and Matrone (9), however, found that excess dietary cadmium greatly increased the zinc concentration of the testes of mice when dietary copper levels were low but increased it only slightly when copper levels were adequate. Kidneys. The trace-element composition of the kidneys is shown in table 9. The copper concentration in the kidney was significantly greater in the 30 and 60 /¿g Cd/g groups than in the controls. Schroeder and Nason (23) and Anke et al. (20, 24) reported similar results for rats, swine, ducks, and hens. Dietary cadmium significantly increased the zinc concentration of the kidneys in the 15, 30, and 60 /¿gCd/g groups compared with that of controls. This response would appear to be a general one applicable to many species (4, 6, 9, 20). The data presented show positive inter actions between cadmium and copper, iron, zinc, and manganese. The elevated and decreased levels of these elements in some organs and tissues may be a direct effect by cadmium on absorption and/or storage and excretion. Previously published data (8) has shown that the lambs fed 60 fig Cd/g had a negative zinc balance rela tive to controls ( -5.88 vs. +4.20 /¿g/lamb/ day). Hence, the elevated liver and kidney values for zinc in the cadmium group must be due to withdrawal of zinc from tissues

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other than those reported in this paper. Anke et al. (24) has shown that high levels of dietary cadmium significantly depleted the concentration of zinc in muscles, bones, and feathers of hens while significantly in creasing the liver stores of this element. Hence, one can hypothesize that cadmium displaced zinc from the muscle and bone of the lambs, and this in turn increased blood zinc, which increased liver zinc. In turn, higher blood zinc levels increased kidney zinc levels as zinc was not signifi cantly increased in the urine. It seems probable that the increased liver zinc in duced the production of metallothionein and acted as a protective effect against the cadmium ( 14 ). However, the involvement of metallothionein in heavy metal intoxica tion in the liver is open to some doubt (39). As the metalloprotein in the liver is believed to be a zinc sink (40), the in creased zinc level is believed to have de creased the copper, iron, and manganese levels due to decreased binding sites on the protein. While it seems possible that cadmium disrupts the absorption of copper, iron, and manganese, previously published data (8) on the same animals showed that cadmium had only a slight effect on the apparent absorption of iron. The intestinal absorp tion of copper appears to be mediated by metallothionein (37). In the liver, the ap parent metallothionein-regulated intracellular metabolism of copper ( 38 ) may be dis rupted. The decrease in copper concentra tion in the liver and in ceruloplasmin synthesis (25) may reflect this disruption. Finally, it is apparent from the data pre sented here and that from Mills and Dal-

CADMIUM

IN OVINE TISSUES

garno's (25) work that dietary cadmium at low concentrations can cause serious de rangements in copper metabolism. Increas ing the zinc:cadmium ratio in the diet may be useful in overcoming this effect. In addition, the feeding of low levels of cad mium to the lambs caused marked accumu lation of this metal in liver and kidneys, hence causing doubt on the suitability of these organs for human consumption when the animals are produced in areas subject to cadmium contamination. LITERATURE CITED 1. Friberg, L., Piscator, M. & Nordberg, G. (1971) In: Cadmium in the Environment, pp. 27-139. CRC Press, Cleveland. 2. Flick, D. F., Kraybill, H. F. & Dimitroff, J. (1971) Toxic eftects of cadmium: a review. Environ. Res. 4, 71-85. 3. Vallee, B. L. & Ulmer, D. D. (1972) Bio chemical effects of mercury, cadmium and lead. Annu. Rev. Biochem. 41, 91-128. 4. Powell, G. W., Miller, W. J., Morton, J. D. & Clifton, C. M. (1964) Influence of dietary cadmium level and supplemental zinc on cad mium toxicity in the bovine. J. Nutr. 84, 205214. 5. Supplée,W. C. ( 1961 ) Production of zinc deficiency in turkey poults by dietary cad mium. Poult. Sci. 40, 827-828. 6. Cousins, R. T., Barber, A. K. & Trout, J. R. ( 1973 ) Cadmium toxicity in growing swine. J. Nutr. 103, 964-972. 7. Hill, C. H., Matrone, G., Payne, W. L. & Barber, C. W. (1963) In vivo interactions of cadmium with copper, zinc and iron. J. Nutr. 80, 227-235. 8. Doyle, J. J., Pfander, W. H., Grebing, S. E. & Pierce, J. O., II. (1974) Effect of dietary cadmium on growth, cadmium absorption and cadmium tissue levels in growing lambs. J. Nutr. 104, 160-166. 9. Bunn, C. R. & Matrone, G. (1966) In vivo interactions of cadmium, copper, zinc and iron in the mouse and rat. J. Nutr. 90, 395-399. 10. Banis, R. J., W. G., Dietary Walker, cadmium, E. F. & O'Connor, J. Pond, R. (1969) 11. 12.

13. 14. 15.

iron and zinc interactions in the growing rat. Proc. Soc. Exp. Biol. Med. 130, 802-806. Fox, M. R. & Fry, B. E. (1970) Cadmium toxicity decreased by dietary ascorbic acid supplements. Science 169, 989-991. Gunn, S. A., Gould, T. C. & Anderson, W. A. ( 1968 ) Mechanisms of zinc, cysteine and selenium protection against cadmium-induced vascular injury to mouse testis. J. Reprod. Pert. 15, 65-70. Parizek, J. ( 1957 ) The destructive effect of cadmium ion on testicular tissue and its pre vention by zinc. J. Endocrinol. 15, 56-63. Webb, M. ( 1972) Protection by zinc against cadmium toxicity. Biochem. Pharmacol. 21, 2767-2771. Kar, A. B. & Kamboj, V. P. (1965) Cad

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16.

17.

18. 19.

20.

21.

22.

23.

24.

25.

26.

27. 28. 29.

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Interactions of cadmium with copper, iron, zinc, and manganese in ovine tissues.

Diets containing 0, 5, 15, 30, and 60 ppm of cadmium were fed to male lambs for 191 days to ascertain what effect cadmium might have on the tissue con...
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