The Significant Advances of the Past Fifty Years in Poultry Nutrition*

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minds and draw conclusions. He was positive without being dogmatic. He was always constructive. He was a family man justly proud of the accomplishments of members of that family. His passing creates a void. He will be missed by many. He will be remembered. In his passing we have lost a friend." H. D. BRANION J. R. CAVERS

Ontario Agricultural College Guelph, Ontario, Canada

The Significant Advances of the Past Fifty Years in Poultry Nutrition* L. C. N O R R I S

Department of Poultry Husbandry, Cornell University, Ithaca, N. Y. EARLY DEVELOPMENTS

A T THE time the Poultry Science -**• Association was organized at Cornell University in 1908, the science of poultry nutrition as it is known today had been born but had made little growth. The birth was attended by Eijkman (1897), a Dutch physician at the Institute of Pathology, Batavia, Java, who observed during controlled experimentation with chickens a syndrome similar to beri-beri in humans which he designated polyneuritis gallinarum. The syndrome was caused by the continued consumption of polished rice but failed to develop when unpolished rice or rice polishings were fed. Eijkman believed that the factor causing polyneuritis was a toxic substance formed in the digestive tract in the absence of a preventive factor in rice polishings. Grijns (1901), Eijkman's successor at * This is the second in a series of review articles being published in celebration of the fiftieth anniversary of the Poultry Science Association.

Batavia, in further work with chickens concluded that rice polishings contain very small quantities of an essential nutrient of unknown composition which, when present in the diet, prevents the development of polyneuritis. Eijkman (1906) abandoned the toxin hypothesis and stated in agreement with Grijns that polyneuritis is caused by a lack of a substance different in nature from protein, fat, carbohydrates or minerals. Thus polyneuritis gallinarum appears to be the first clearly characterized nutritional deficiency disease experimentally produced. Funk (1913, 1914) made use of 14-day old chicks in studies of the effect of various diets on the growth of Rous's sarcoma. Chicks fed a diet composed of unpolished rice failed to grow and died within a period of two months. After that time, according to Funk and Macallum (1914), some of the chicks fed the control diet in the earlier work developed a "rachitisartige Erkrankung." Funk and Macallum added

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never looked back. As a teacher he inspired thousands, as a scientist in the field of nutrition he served mankind. These things we knew. But it was the constant flashes of the rare philosophical mind for which we liked him best. All his attributes were the result of his interest in people. He enjoyed discussion. He stimulated and enriched the discussion. He had an extensive knowledge and he was never frugal with it. He could be critical but in a friendly way. He could look into men's

FIFTY YEARS IN POULTRY NUTRITION

Buckner, Nollau and Kastle (1916) fed chicks a few days old grain mixtures of high and low lysine content under controlled conditions. Two experiments were conducted. At the end of the experiments the chicks fed the high lysine diet had average weights of three to three and onehalf times those fed the low lysine diet. Buckner and associates concluded that in

all probability lysine is required for rapid growth of chickens. This finding was confirmed by Osborne and Mendel (1916). They pointed out, however, that the analyses of Buckner and associates were not sufficiently accurate to show the lysine content of their diets but that they differed considerably in this amino acid, in view of what was known about the lysine content of the seeds used in them. Hart, Halpin and Steenbock (1917) reported that chickens placed on experiment at less than half normal weight make slow growth and maintain themselves when fed a diet restricted to corn meal, corn gluten feed and calcium carbonate. On the other hand chickens fed a diet restricted to wheat meal, wheat gluten and calcium carbonate died within three months. Modifying the wheat ration by the addition of a complex salt mixture, or this addition together with the substitution of casein for a part of the wheat protein, did not appear to improve the nutritive value of the wheat grain for young growing chickens. Only when butter fat, previously shown by McCollum and Davis (1913) and Osborne and Mendel (1913) to contain an essential nutrient for the rat, was added to the ration, did growth take place and the chickens show evidence of wellbeing. Osborne and Mendel (1918), encouraged by their success in showing that the chick requires lysine, continued attempts to adapt the chick for use as an experimental animal. In this work many of the chickens developed a characteristic leg weakness, presumably similar to the "rachitisartige Erkrankung" of Funk and Macallum (1914) and the "weakness in the legs" of Drummond (1916). Osborne and Mendel, however, obtained some degree of success which they attributed to the consumption of the blotting paper with which the bottoms of the chick cages

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cod liver oil to the unpolished rice diet, as a consequence of work conducted previously by Osborne and Mendel (1914). Chicks fed this diet also failed to grow, but lived on indefinitely. Funk and Macallum believed that their observations, particularly the arrested growth of the chicks fed the unpolished rice diet, indicated the existence of a growth-vitamin not identical with the vitamin that protects against beri-beri. Drummond (1916) also attempted to use the chick in a study of the effect of diet upon the growth of Rous's sarcoma. He concluded from his results that the young chick when kept under artificial conditions is not a suitable subject upon which to conduct experiments in the study of growth. This was based upon the observation that many young chicks, fed a regular diet which under better surroundings promoted normal development, showed periods of arrested growth, the same as chicks fed a diet of unpolished rice. Moreover, cases of leg weakness developed both in the chicks fed the regular diet and in those fed the experimental diet. Because of these observations, Drummond stated that the previous work of Funk and Macallum (1914) afforded no satisfactory evidence of the existence of any accessory substances, or vitamins. Funk (footnote, 1916) stated that on improving the diet of the regularly fed chicks he had obtained new data confirming previous statements on the effect of unpolished rice in arresting the growth of young chickens.

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During the latter part of this era the terminology of the unknown substances essential for adequate nutrition was in a highly confused state. Hopkins (1912) called them the "accessory factors." Funk (1912) named the substance which prevents beri-beri in man and polyneuritis in chickens the beri-beri vitamine, and the one which prevents experimental scurvy in

animals and scurvy in infants the scurvy vitamine, because he believed that these were organic bases necessary for the maintenance of life processes. McCollum and Kennedy (1916) suggested that the term "vitamine" be discontinued, and the terms "fat-soluble A" and "water-soluble B " be applied to the two classes of unknown substances that induced growth. Drummond (1920) reconciled the existing confusion in terminology of recommending that the letter " e " in "vitamine" be dropped, since no evidence existed that vitamins were organic bases, and that the unknown substances required for growth, the prevention of beri-beri and the prevention of scurvy be called respectively vitamins A, B and C. "LEG WEAKNESS" PREVENTED BY VITAMIN D

Emmett and Peacock (1922, 1923) reported that in the absence of vitamin A chicks developed xerophthalmia, leg weakness and beading of the ribs. Hart, Halpin and Steenbock (1922) in further studies on leg weakness in chicks showed that it was prevented by supplying the vitamins of cod liver oil. The findings of these investigators were confirmed by Mitchell, Kendall and Card (1923). Bethke and Kennard (1924) reared chicks to maturity indoors by supplying either cod liver oil or fresh egg yolk, and obtained a considerable number of eggs from the pullets. McCollum and associates (1922) reported that the vitamin A activity of cod liver oil was composed of two components. One component, designated vitamin D, was found to prevent rickets in rats; the other continued to be called vitamin A. In view of this discovery, leg weakness in chicks was correctly assumed to be due to vitamin D deficiency. Hart and associates (1923) reported that exposure to ultraviolet light prevented leg weakness in

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were lined, and to paper fiber supplied in subsequent experiments. Hart, Halpin and Steenbock (1920) described experiments on leg weakness in chicks fed synthetic diets containing all the known nutrients on which rats thrive. Following the report of Osborne and Mendel (1918), a study of sources of bulk was included in the investigation. Some success was attained when finely ground paper was added to the diet. The paper was thought to prevent the absorption of a toxic substance which caused leg weakness. The work of Hart, Halpin and Steenbock (1920) ended the first era in the development of the present-day science of poultry nutrition. In this era partial success was obtained in adapting the chick to controlled laboratory conditions, but the cause of leg weakness, the chief difficulty preventing complete success, was not revealed. Chickens were shown to require an unknown food substance which prevents the development of polyneuritis and lysine was shown to be needed for the rapid growth of chicks. Evidence was also obtained by feeding diets composed of unpolished rice and cod liver oil, or the entire wheat plant and butter, that these fats contained an unknown substance required by the chick. Finally observations were made which were believed to indicate that the chick required other unknown substances in addition to the one preventing polyneuritis and the one present in some fats.

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"NUTRITIONAL LEG PARALYSIS" CAUSED BY RIBOFLAVIN DEFICIENCY

Norris, Heuser and Wilgus (1930) and Norris and associates (1931) described a curious paralysis of the legs of chicks which was prevented by a protein-free, low-lactose concentrate prepared from milk. Hogan, Guerrant and Kempster (1925) reported a similar type of paralysis obtained in chicks fed synthetic diets but called it polyneuritis. Norris and associ-

ates showed, however, that the paralysis was not due to a deficiency of vitamin B. They also concluded that it was probably not caused by a deficiency of vitamin G. At that time vitamin G was considered to be the anti-pellagra vitamin as it prevented a pellagra-like dermatitis in rats. Ringrose, Norris and Heuser (1931) and Ringrose and Norris (1934) believed that they had resolved the uncertainty regarding the need of the chick for vitamin G by showing that in chick nutrition the vitamin was a complex composed of a factor which prevented nutritional leg paralysis and a factor that prevented a dermatitis not previously observed in this species. Very shortly, however, the former was found to be the vitamin G of the rat and the latter was designated the chick antidermatitis factor. Bethke, Record and Kennard (1931) confirmed the observations of Norris and associates (1930, 1931) on nutritional leg paralysis and also obtained evidence of the complex nature of vitamin G. Heiman, Sullivan and Norris (1934) found that vitamin G deficiency in chicks was due to the lack of the yellow pigment present in milk which was eventually named riboflavin. This was confirmed by Norris, Davis and Sullivan (1935) and by Lepkovsky and Jukes (1935, 1936). Heiman and Norris (1933), Bethke, Record and Kennard (1933) and Halpin, Holmes and Hart (1933) reported that vitamin G is required for hatchability. Heiman (1935) and Norris and associates (1936) presented further evidence on the need of this vitamin for hatchability, including evidence of a correlation between the hatchability of eggs and the riboflavin content of egg white. At about the time that milk products were found to be good sources of vitamin G for feeding poultry, nutritional leg paralysis was observed on poultry farms

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chicks and thus substituted for vitamin D in poultry nutrition. Hart and associates (1925) found that ultraviolet light also promoted greater egg production, higher hatchability and increased strength of egg shells. The discovery that vitamin D prevents leg weakness in chicks led within a few years to the almost universal use of cod liver oil in poultry feeds. Through its use it became possible to rear chicks without regard to seasonal variation, and to keep hens in quarters which prevented exposure to the rigors of severe winter weather. Without it the present day poultry industry would not have developed. The need of chickens for vitamin A independent of vitamin D was established by Beach (1923, 1924) and Hart and associates (1924). Hauge and Carrick (1927) showed that the vitamin A requirement of growing chicks was adequately met by supplying yellow corn. This provided further confirmation of the correlation between the pigments of yellow corn and "fat-soluble vitamine" reported by Steenbock and Boutwell (1920). Kline, Schultze and Hart (1932) found that carotene, but not xanthophyll, possessed vitamin A activity for the chick. These findings on vitamin A and materials possessing vitamin A activity led to the almost complete disappearance of vitamin A deficiency on poultry farms.

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ENCEPHALOMALACIA FOUND TO BE VITAMIN E DEFICIENCY

Pappenheimer and Goettsch (1931) observed in the brains of chicks a necrosis of nutritional origin. Pappenheimer and Goettsch (1934) reported that protection against the disorder which they named encephalomalacia was afforded by certain vegetable oils. At the same time these studies were being made the disease was occurring on poultry farms. Poultrymen called it the "crazy chick disease." A report on the occurrence of field encephalomalacia was made by Jungherr (1936). Dam and associates (1938) found that the disease was caused by vitamin E deficiency. Although encephalomalacia was the cause of some loss in broiler production between 1930 and 1950, it is only in the last few years that the disease has become of practical importance. This appears to be due in part to the development of high energy rations containing large amounts of corn. Singsen and associates (1954) reported that the development of encephalomalacia in chicks is related to the vitamin E content of breeder diets as well as to the vitamin E content of chick diets. Singsen and associates (1955) and Bunnell and associates (1955) also reported that several antioxidants were effective in preventing the development of encephalomalacia. Among these were diphenyl-pphenylenediamine (DPPD), 2,6-di-tertiary butyl-4-methyl phenol (BHT) and l,2-dihydro-2,2,4-trimethyl-6-ethoxyquinoline (Santoquin). Previously Dam and associates (1951) had reported that methylene blue afforded complete protection against this disorder. Scott (1953) showed that vitamin E was concerned in the prevention of the enlarged hock disorder of poultry. These findings emphasized the importance of maintaining an

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in New York State. The popular name given the condition was "curly-toed paralysis." The discovery of the cause of nutritional leg paralysis and its appearance on poultry farms led first to the almost universal use of milk products in chick starting rations and in rations for breeders, and then, upon the development of appropriate industries, to the use of riboflavin manufactured by chemical synthesis and fermentation procedures. Norris and Ringrose (1935) and Ringrose and Norris (1936a, b) showed that the dermatitis observed by them in 1931 was a complex deficiency disease which, depending upon type and treatment of diet, developed as a consequence of a deficiency of either one or the other of two factors. When pantothenic acid was isolated by Williams and associates (1938), Jukes (1939) obtained a small supply from them and showed that the dermatitis studied by Norris and Ringrose (1935) and Ringrose and Norris (1936b) was due to a lack of this vitamin. The cause of the dermatitis studied by Ringrose and Norris (1936a) was shown by Hegsted and associates (1942) to be due to a deficiency of biotin. Both pantothenic acid and biotin have been synthesized by the chemical manufacturing industry, but only pantothenic acid is being used to anygreat extent in the manufacture of poultry feeds. The use of pantothenic acid is due to the results of studies on the quantitative pantothenic acid requirement of chicks and hens and determinations of the pantothenic acid content of feedstuffs which show that present day high energy poultry rations are borderline in this vitamin. Evidence of a deficiency of pantothenic acid in the diet of breeder hens, which causes excessive mortality in newly hatched chicks, has been reported by Fisher and Hudson (1956).

FIFTY YEARS IN POULTRY NUTRITION

adequate supply of vitamin E in poultry rations. This has been accomplished by means of highly concentrated preparations of natural or synthetic vitamin E or by the use of antioxidants.

PEROSIS DUE TO INSUFFICIENT MANGANESE

Gallup and Norris (1938) and Caskey, Gallup and Norris (1939) observed by xray examination and physical measurements that the bones of chicks fed a manganese deficient diet were thickened and shortened. The ash content of the bones was also slightly but significantly reduced but from x-ray examination and staining

with silver nitrate calcification appeared to be normal. The results showed that manganese was required for bone formation in general and not just for prevention of perosis. Evidence obtained by Wiese and associates (1939, 1941) and Combs, Norris and Heuser (1942) showing that bone phosphatase is reduced in manganese deficiency in the chick, supported this conclusion. In 1934 van der Hoorn, Branion and Graham (1938) obtained evidence that manganese is required for the maintenance and growth of chicks. Wilgus, Norris and Heuser (1937) and Gallup and Norris (1937b) also showed that manganese is required for chick growth. Lyons and Insko (1937) and Gallup and Norris (1937b, 1939) reported that manganese in the diet of hens results in subnormal hatchability, characterized by high embryonic mortality during the last few days of incubation. Lyons and Insko observed typical symptoms of chondrodystrophy in the embryos, including shortened wing and leg bones and globular heads. These workers and Caskey and Norris (1938), Norris and Caskey (1939) and Caskey, Norris and Heuser (1944) found that chicks from some hens fed a manganese deficient diet suffered from extreme nervousness, head tremors and head retractions. In an exceedingly short time after the discovery that manganese prevents perosis in chicks, feed manufacturers in general began adding manganese to chick and breeder rations with the result that slipped tendon disappeared for the most part and the danger of poor hatchability from a slight insufficiency of this mineral was eliminated. The discovery was particularly important to the broiler industry as it made it possible to eliminate one of the greatest causes of loss then prevailing.

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Shortly after the discovery that vitamin D prevents leg weakness in chicks, poultrymen who reared chicks indoors began to have losses from a condition called slipped tendon which crippled the chicks. In aggravated cases the Achilles tendon slipped from the condyles of the tibia of the leg and made the leg useless. Hunter and Funk (1930) and Payne, Hughes and Leinhardt (1932) showed that slipped tendon could be produced experimentally by supplying high levels of calcium and phosphorus in the chick diet. Titus and Ginn (1931) and Titus (1932) applied the name perosis (deforming leg weakness) to the deformity and showed that rice bran is a preventive. Sherwood and Couch (1936) obtained similar effects with wheat gray shorts and Sherwood and Fraps (1936) reported that the preventive effect of wheat gray shorts on perosis was due to one or more of the mineral constituents of the ash of this product. Wilgus, Norris and Heuser (1936a, 1937) demonstrated that slipped tendon is due largely to a deficiency of manganese. This finding was confirmed by Gallup and Norris (1937a), Heller and Penquite (1937), and others.

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The finding that choline is required for the prevention of perosis in addition to manganese has led to the rather general use of added choline in poultry rations, although the available evidence indicates that practical ingredients frequently supply adequate amounts of this vitamin. The question, however, is unsettled and further experimentation is required to determine the choline requirements of poultry, particularly as the requirement is related to the presence of choline precursors in practical ingredients, and the supply of vitamin B12, which has been shown by Schaefer, Salmon and Strength (1949) and Gillis and Norris (1949a, b) to exert a sparing effect on choline. Briggs and associates (1943) discovered that chicks suffering from niacin deficiency developed perosis in addition to other symptoms. Somewhat later, Briggs (1946) found that perosis occurred in

niacin deficiency in turkey poults. Scott and Heuser (1952) showed that niacin deficiency was responsible for a bowed leg condition in ducklings and Battig and associates (1953) observed that niacin prevented perosis in goslings. Scott (1953) reported that niacin is required along with vitamin E to prevent a form of enlarged hocks in turkey poults similar to that encountered on poultry farms. These findings established the importance of niacin in bone development in chicks, turkey poults, ducklings and goslings. The results of Childs, Carrick and Hauge (1952), Sunde (1953), and Patterson and associates (1956) indicate that most chick rations contain sufficient niacin to meet the requirements. VITAMIN B:2 AND THE "ANIMAL PROTEIN FACTOR" Following the isolation of vitamin B12 by Rickes and associates (1948), Ott, Rickes and Wood (1948) showed that vitamin B12 promoted growth in chicks which had been fed diets lacking this vitamin. Lillie, Denton and Bird (1948) found that vitamin B12 and the animal protein factor were related. Bird (1950) and Milligan, Arscott and Combs (1952) reported that chicks hatched from the eggs of vitamin Bi2-depleted hens suffered severe mortality when fed a diet lacking in this vitamin. Miller, Norris and Heuser (1956), however, obtained no evidence of this in depleted chicks used in studies on the vitamin B12 requirement. Yacowitz and associates (1952) found that an all-vegetable diet containing 25% protein resulted in more rapid depletion of vitamin B12 reserves of hens than a similar diet containing 16% protein. This is in accord with the finding of Rubin and Bird (1947) that a high level of soybean oil meal increased the requirement for the animal protein factor. Lillie, Olsen and Bird (1949) obtained

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PEROSIS CAUSED BY LACK OF CHOLINE AND NIACIN Following the demonstration that slipped tendon or perosis in chicks is prevented for the most part by the addition of manganese to the ration, Jukes (1940a) showed that perosis both in turkey poults and chicks is also produced by choline deficiency, even though the ration is adequate in manganese. This was confirmed by Hegsted, Mills, Elvehjem and Hart (1941) and by Hogan, Richardson, Patrick and Kempster (1941). McGinnis, Norris and Heuser (1944) reported that betaine, methionine or choline prevented perosis and promoted growth in chicks when added to a diet composed of both purified and crude ingredients, but that only choline was effective when a purified diet containing gelatin was fed. Their findings were contrary to the findings of Jukes (1940b) who showed that betaine was ineffective in preventing perosis in turkey poults fed a semi-purified diet containing some crude ingredients.

FIFTY YEARS IN POULTRY NUTRITION

The research work on vitamin B12 showed that it was a part at least of the animal protein factor previously known to be required both for growth and for reproduction, and found in meat and fish

products. The discovery of the importance of vitamin B12 in poultry nutrition led to the early development of crude sources of this vitamin of standardized potency. As a consequence poultry rations can be made adequate in this vitamin with much greater assurance than was possible when it was necessary to depend upon animal products as sources of the animal protein factor. The discovery of the value of vitamin B12 in poultry nutrition represents another important step forward in developing better poultry rations. ANTIBIOTICS FOUND TO BE GROWTH STIMULATING The discovery that vitamin B12 is required for chick growth led Stokstad and associates (1949) to study the value of crude sources of the vitamin. They found that not all of the activity of crude sources of the vitamin could be explained on the basis of vitamin B12 content, and postulated that the animal protein factor was multiple in nature. Stokstad and Jukes (1950) showed that the second factor in crude sources of vitamin Bi2 was the antibiotic, aureomycin. Similar findings were also obtained by Whitehill, Oleson and Hutchings (1950). Previously Moore and associates (1946) reported that streptomycin stimulated the growth of chicks, but their findings were overlooked. Harned and associates (1949) reported that aureomycin promoted chick growth but believed that the effect was probably due to the elimination of an infection. In the work of Stokstad and Jukes (1950), however, no infections were noted during the course of the experimental work. Coates and associates (1952) found that procaine penicillin added to a diet of practical type promoted increased growth, in chicks housed in a laboratory in which poultry had been kept for ten years. Chicks from the same hatch housed in two other laboratories previously unused for

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evidence that vitamin B12 is required for reproduction in poultry. More direct evidence of this was obtained by Petersen and associates (1950) and Peeler and associates (1951). Miller, Norris and Heuser (1956) and Chin and associates (1958) presented the results of extensive studies on the vitamin B12 requirements of chickens, and reviewed the previous work of other investigators. McGinnis, Hsu and Graham (1948) reported that blood non-protein nitrogen content was higher in chicks deprived of the animal protein factor than in normal controls. Charkey and associates (1950) confirmed this observation in studies on the non-protein nitrogen components of chick blood, and concluded that vitamin B12 enhances amino acid utilization in the chick. Jukes and Stokstad (1952) reported that vitamin B12 is required for the transfer of methyl groups from choline or betaine to homocystine to form methionine in studies with vitamin Bi2-deficient chicks. The work of Stekol, Hsu, Weiss and Smith (1953) and that of Young, Norris and Heuser (1954) showed that vitamin B12 is required for the synthesis of methyl groups in the chick, but no evidence was obtained in this work that the vitamin takes part in the methylation of homocystine. Schaefer, Salmon and Strength (1949) and Gillis and Norris (1949b) showed that vitamin B12 exerts a sparing effect on the requirement of the chick for methylating compounds. Briggs, Hill and Giles (1950) found that methionine and choline spared the requirement of chicks for vitamin Bi2. Yacowitz, Norris and Heuser (1951) reported that vitamin B12 spares the requirement of the chick for pantothenic acid.

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rearing poultry grew as well on the diet the requirement for manganese, and without penicillin as when it was included Lindblad and associates (1952) obtained in the diet. Somewhat similar findings findings which suggested that aureomycin were made by Bird, Lillie and Sizemore improves the utilization of calcium and (1952) and by Hill, Branion and Slinger phosphorus. Ross and Yacowitz (1952) (1952). These findings suggested that the observed increased bone calcification on depression in growth obtained in chicks supplying penicillin to chicks fed low housed in previously used quarters was levels of vitamin D. A possible explanacaused by an unrecognized infection ordi- tion of the improved utilization of minnarily transmissible but controlled by erals was provided by the work of Andersupplying antibiotics. son, Slinger and Pepper (1952) who found Antibiotics also appear to exert a spar- that supplying procaine penicillin to ing effect on some nutrients. Oleson, chicks decreases the pH of the cecal Hutchings and Whitehill (1950) reported contents. Heuser and Kosikowsky (1952) that the requirement of the chick for vi- obtained evidence that procaine penicillin tamin B12 was reduced by including aureo- decreases the pH content of the small mycin in the diet. This observation was intestine. A decrease in the pH of the conconfirmed by Stokstad and Jukes (1951). tents of the intestinal tract would unBiely and March (1951) found that aureo- doubtedly favor an increase in the absorpmycin replaced riboflavin, niacin and folic tion of relatively insoluble minerals such acid in a semi-purified chick diet but had as calcium, phosphorus and manganese, no growth promoting effect if the diet con- by increasing their solubility. tained these vitamins. Waibel, Sunde and These discoveries led to the general use Cravens (1952) showed indirectly that of antibiotics in rations for chicks, penicillin exerts a sparing effect on biotin broilers and turkey poults. Their use has and folic acid by finding increased quanti- made it possible for poultrymen to obtain ties in the eggs of hens fed the antibiotic. greater and more uniform growth and Common and associates (1950) discovered better feed efficiency. Antibiotics have indirectly that aureomycin spares ribo- thus proven to be of great practical sigflavin by finding an increased quantity of nificance. the vitamin in the blood stream of pullets following administration of the antibiotic. THE FIELD HEMORRHAGIC SYNDROME Matterson and Singsen (1951) and Heuser AND VITAMIN K DEFICIENCY and Norris (1952) observed that aureoDam (1935a, b) and Almquist and mycin, bacitracin, penicillin and terramy- Stokstad (1935a, b) demonstrated in excin exert a sparing effect on an unidenti- perimental work with chicks the existence fied factor or factors present in fish prod- of a new vitamin present in the nonucts, while Scott (1951) showed that saponifiable fraction of some animal and aureomycin spares the requirement of vegetable fats. The name vitamin K was turkey poults for an unidentified factor proposed by Dam (1935a) for the new present in dried brewers yeast. vitamin. Schonheyder (1935) reported Migicovsky and associates (1951) con- that the clotting time of the blood of cluded that under the experimental condi- chicks was enormously increased when a tions penicillin enhances the absorption of deficiency of vitamin K existed in the calcium. Pepper, Slinger and Motzok diet. Almquist and Stokstad (1935b) (1951) showed that aureomycin decreases found dehydrated alfalfa meal to be a

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The great importance of the discovery of vitamin K to the poultry industry was not revealed until research workers obtained evidence that a deficiency of the vitamin was implicated in the development of the "field hemorrhagic syndrome" of the chick. Asplin and Boyland (1947) reported the development of a hemorrhagic syndrome in chicks supplied sulfamethazine in which blood clotting time was increased. This effect was overcome by vitamin K. Delaplane and Milliff (1948) found that the continuous feeding of sulfaquinoxaline caused hemorrhages beneath the skin of the legs and in the combs of pullets in egg production, followed by death. Gordon (1951) observed the development of a hemorrhagic syndrome in a flock of pullets following treatment for coccidiosis with sulfaquinoxaline. In repeated experiments, a definite connection was established between sulfaquinoxaline and the development of the hemorrhagic syndrome. The syndrome was observed by Goldhaft and Wernicoff (1954) in a flock of White Leghorn pullets on range in New Jersey; Gray, Snoeyenbos and Reynolds (1954) in chickens which they

autopsied; and Cover, Mellen and Gill (1955) in broiler chicks in the Delmarva area of Delaware. The symptoms of the hemorrhagic syndrome were similar to the previously described symptoms of vitamin K deficiency except that in the hemorrhagic syndrome hypoplastic bone marrow was observed. Cover, Mellen and Gill (1955) found that chicks fed a corn-soybean meal ration developed pale, grossly abnormal bone marrow when sulfaquinoxaline was administered in the drinking water, but not in chicks when the basal ration contained alfalfa meal. Nelson and Norris (1956) observed hypoplastic bone marrow in chicks fed a diet lacking in vitamin K, either with or withotft added sulfaquinoxaline. Griminger and associates (1953) reported that terramycin and 3-nitro-4hydroxy phenylarsonic acid significantly prolonged blood clotting time of chicks fed a vitamin K-low diet. Vitamin K reduced the blood clotting time to normal when added at a curative level. The results of these investigators on terramycin were not confirmed by Reynolds, Warden and Luther (1953-1954) or Sweet, Romoser and Combs (1954), but the latter workers showed that para amino phenylarsonic acid significantly increased the blood clotting time of chicks fed a corn meal-soybean meal diet. The condition was overcome with either menadione or alfalfa meal. Frost and Spruth (1955) reported, on the other hand, that they were unable to show that para amino phenylarsonic acid delayed blood clotting time. Sweet, Romoser and Combs (1954) found that sulfaquinoxaline significantly delayed blood clotting time in chicks, confirming results observed previously in other animals with sulfonamides by Black and associates (1942) and others. Similar results were obtained by Shelton and co-

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good source of vitamin K and these same workers (1937) observed that soybean oil contains the vitamin. Almquist and Stokstad (1935b) also found that vitamin K was formed by bacterial action in fish meal and rice bran allowed to stand for several days in a wet condition, and Almquist, Pentler and Mecchi (1938) reported the results of a study on bacteria which produced this vitamin. These findings apparently explained the difficulty involved in using animal protein supplements of uncertain origin in studies on vitamin K deficiency. Almquist and Klose (1939a, b) reported that 2-methyl-l,4-naphthoquinone, later named menadione, was more potent than vitamin Ki in preventing vitamin K deficiency.

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Goldhaft and Wernicoff (1954), Bornstein and Samberg (1954) and Frost and Spruth (1955) reported prolonged blood clotting time in field hemorrhagic disease which was corrected by adding menadione sodium bisulfite to the drinking water. Gray and associates (1954) also observed delayed blood clotting time in this disease but Cover, Mellen and Gill (1955) found blood clotting time to be normal. Nelson and Norris (1956) observed hemorrhages in chicks supplied sulfaquinoxaline and limited quantities of menadione in which blood clotting time was normal. Larger quantities of menadione prevented the development of hemorrhages. Although the evidence that vitamin K deficiency is implicated in the field hemorrhagic syndrome is conflicting, the use of synthetic vitamin K preparations in poultry rations has increased greatly during the past few years and the "field hemorrhagic disease" has disappeared for the most part. ENERGY REQUIREMENTS AND ENERGYPROTEIN RELATIONSHIPS

Heuser and associates (1945) called attention to the better growth, greater egg production, and improved feed effi-

ciency obtained by feeding rations of low fiber content. The greater efficiency of the low fiber rations appeared to be due to the larger amount of digestible nutrients in them. Scott, Matterson and Singsen (1947) reported that better growth and feed efficiency were obtained by feeding broilers high energy rations. Similar results were obtained by Scott, Heuser and Norris (1948) with turkey poults, and Singsen, Matterson and Kozeff (1950) with layers. These reports interested research workers in studying the energy requirements of chicks. Robertson and associates (1948) presented results which indicated that White Leghorn chicks required for satisfactory growth a ration containing approximately 800 Calories of productive energy per pound of feed. Panda and Combs (1950) obtained evidence which indicated that 850 Calories per pound of ration was sufficient to promote rapid growth in New Hamsphire chicks. The high energy ration reported by Scott, Matterson and Singsen (1947) contained about 1,000 Calories per pound of ration. Hill and Dansky (1954) found that maximum growth in Red Rock crossbred chicks as determined by weight was obtained on feeding rations containing as little as 625 Calories per pound when the low calorie content was obtained by diluting the ration with pulverized oats. The greatest fat deposition in the bodies of the chicks was obtained, however, when the undiluted ration containing 970 Calories per pound was fed. The energy content of the experimental diets used in the experiments of these investigators were calculated from the data of Fraps (1946) on the productive energy content of poultry feeds. As a consequence of the findings on the value of high energy rations and the energy requirement for growth the quantitative relationship between the available

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workers (1954), Frost and Spruth (1955), Yacowitz and associates (1955), Cover, Mellen and Gill (1955) and Nelson and Norris (1956). These research workers found in general that the prolonged blood clotting time was corrected either with menadione, menadione sodium bisulfite or alfalfa meal. Cover, Mellen and Gill (1955), however, observed no correlation between the use of sulfaquinoxaline and the occurrence of the field hemorrhagic syndrome. According to Norris and Nelson (1955) this is explainable in view of recent dietary changes and changes in processing of feedstuffs which have reduced the vitamin K content of presentday poultry rations.

FIFTY YEARS IN POULTRY NUTRITION

As a consequence of the work on the energy requirements of poultry and the relationship of the protein requirement to the energy content of the rations, the poultry industry has turned in general to the use of high energy rations, especially for producing broilers and rearing growing chicks, and also to a considerable extent for producing eggs. This has been one of the most striking developments in poultry nutrition in recent years, and has led to improved profits for poultry producers. INDISPENSABLE AMINO ACIDS AND SOYBEAN OIL MEAL

The extensive use of soybean oil meal iri poultry rations stimulated the experi-

mental work on means of improving the quality of the product. Wilgus, Norris and Heuser (1935) showed that the relative protein efficiency of ground raw soybeans, compared to casein as 100, was 58, while that of soybean oil meal produced by the hydraulic process was 85 and that produced by the expeller process was 89. Wilgus, Norris and Heuser (1936b) and Hay ward and associates (1937) showed that proper heat treatment was essential to produce soybean oil meal of good quality for feeding poultry. Hayward and Hafner (1940) found that supplementing raw soybeans with methionine or cystine improved the protein quality of the beans. No additional improvement was obtained by a combination of methionine and cystine. Autoclaving the soybeans increased the nutritional value of the protein fraction in much the same manner as the methionine and cystine supplements to the raw soybeans, but additions of either cystine, methionine or a combination of the two amino acids to autoclaved soybeans stimulated an even greater response. Almquist and associates (1942) reported that the principal growth limiting deficiency in raw soybean protein is that of methionine. They found also that heated soybean protein is slightly deficient in methionine for the chick at the 20% protein level but is complete in respect to all other amino acids required by this species. This conclusion illustrates in a small way the exceedingly great value to the poultry industry of the research work conducted on the amino acid requirements of chickens and turkeys. Much of this work was conducted at the University of California by Almquist (now with the Grange Company, Modesto, California), Grau, Kratzer and their associates. These workers have determined the indispensable amino acids, required by the chick and some of those required by turkey poults and laying hens, and the quantity

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calories in poultry rations and protein content has been studied extensively by Combs and Romoser (1955), Sunde (1956), Donaldson, Combs and Romoser (1956), Ferguson and associates (1957), Miller, Sunde and Elvehjem (1957), Atkinson and associates (1957), Day and Hill (1957), and Hill and Renner (1957). The results of the experimental work showed that the protein requirement of poultry increases as the energy content of the diet increases, and that the requirements, therefore, can no longer be expressed as percentage of the diet but rather should be expressed as energy:protein ratios. The results also showed that the requirement of the chick for 20% protein during early life applies only to diets of medium energy content. The conclusions of these investigators were based largely upon the use of the productive energy values of Fraps (1946). Anderson (1955) showed that the metabolizable energy values of feedstuffs can be determined more precisely and thus are more accurate than the productive energy values determined by Fraps (1946). Hill and Renner (1957) reported values for the metabolizable energy content of many of \he feedstuffs studied by Fraps.

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SUMMARY

I t is obviously impossible in a short review to discuss all the significant basic discoveries in poultry nutrition made during the past fifty years. This review, therefore, has been limited to a consideration of the findings which have had the greatest impact on the poultry industry. No important advances of this character, however, were made during the forepart of this period but it was significant that research workers were partially successful in adapting the chick to controlled experimentation under laboratory conditions. This made it possible in the following years to discover the causes of leg weakness in chicks, nutritional roup or xerophthalmia, nutritional leg paralysis, perosis and encephalomalacia and some of the causes of the field hemorrhagic syndrome. The solution of many of these problems later led to the developments on antibiotics, high energy rations and Calorie-protein relationships, and to the determination of

the requirements of poultry for the indispensable amino acids and the application of this information in making extensive use of soybean meal and in improving poultry rations in general. REFERENCES Almquist, H. J., 1947. Evaluation of amino acid requirements by observations on the chick. J. Nutrition, 34: 543-563. Almquist, H. J., 1952. Amino acid requirements of chickens and turkeys.—A review. Poultry Sci. 31: 966-981. Almquist, H. J., 1957. Proteins and Amino Acids in Animal Nutrition, 4th Ed., U. S. Industrial Chemicals Co., New York, N. Y. Almquist, H. J., and A. A. Klose, 1939a. The antihemorrhagic activity of certain naphthoquinones. J. Am. Chem. Soc. 61:1923-1924. Almquist, H. J., and A. A. Klose, 1939b. Antihemorrhagic activity of 2 methyl-l,4-naphthoquinone. J. Biol. Chem. 130: 787-789. Almquist, H. J., E. Mecchi, F. H. Kratzer and C. R. Grau, 1942. Soybean protein as a source of amino acids for the chick. J. Nutrition, 24:385-392. Almquist, H. J., C. F. Pentler and E. Mecchi, 1938. Synthesis of the antihemorrhagic vitamin by bacteria. Proc. Soc. Exp. Biol. Med. 38: 336-338. Almquist, H. J., and E. L. R. Stokstad, 1935a. Dietary haemorrhagic disease in chicks. Nature, 136: 31. Almquist, H. J., and E. L. R. Stokstad, 1935b. Hemorrhagic chick disease of dietary origin. J. Biol. Chem. 111:105-113. Almquist, H. J., and E. L. R. Stokstad, 1937. Assay procedure for vitamin K (antihemorrhagic vitamin). J. Nutrition, 14: 235-240. Anderson, D. L., 1955. The energy value of poultry feeds. Proc. Cornell Nutr. Conf. for Feed Mfgrs., p. 5-10. Anderson, G. W., S. J. Slinger and W. F. Pepper, 1952. Effect of dietary microorganisms on the growth and cecal flora of chicks. Poultry Sci. 31: 905. Asplin, F. D., and E. Boyland, 1947. Effects of pyrimidine sulfonamide derivatives on the blood clotting system of chicks and the breeding capacity of adult fowls. Brit. J. Pharmacol. 2: 79-92. Atkinson R. L., A. A. Kurnick, T. M. Ferguson, B. L. Reid, J. H. Quisenberry and J. R. Couch, 1957. Protein and energy levels for turkey starting diets. Poultry Sci. 36: 767-773. Battig, M. J., E. G. Hill, T. H. Canfield and H. J. Sloan, 1953. Prevention of perosis in goslings by

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required in the diet. In addition they have shown that increasing the protein content of the diet is not a satisfactory way of meeting the need for an essential amino acid, deficient in the dietary proteins, since in catabolizing the excess protein a portion of the deficient amino acid is also catabolized. The requirement for an essential amino acid, however, has been found not to increase always in proportion to the increase in protein. Grau and Kamei (1950) showed that the requirements for lysine and the sulfur bearing amino acids increases as the protein is increased but at a slower rate. The requirement for the indispensable amino acids also appears to vary with size, age and variety of poultry. The results of the research work on the amino acid requirements of poultry have been reviewed by Almquist (1947, 1952, 1957).

F I F T Y Y E A R S IN P O U L T R Y N U T R I T I O N

The need for manganese in the bone development of the chick. J. Nutrition, 17: 407-417. Caskey, C. D., L. C. Norris and G. F. Heuser, 1944. A chronic congenital ataxia in chicks due to manganese deficiency in the maternal diet. Poultry Sci. 23: 516-520. Charkey, L. W., H. S. Wilgus, Jr., A. R. Patten and F. X. Gassner, 1950. Vitamin B12 in amino acid metabolism. Proc. Soc. Exp. Biol. Med. 73: 21-24. Childs, G. R., C. W. Carrick and S. M. Hauge, 1952. The niacin requirement of young chickens. Poultry Sci. 31:551-558. Chin, D., J. B. Anderson, R. F. Miller, L. C. Norris and G. F. Heuser, 1958. The vitamin B12 requirement of White Leghorn hens. Poultry Sci. 37: 335-343. Coates, M. E., C. D. Dickinson, G. F. Harrison, S. K. Kon, J. W. G. Porter, S. H. Cummins and W. F. J. Cuthbertson, 1952. A mode of action of antibiotics in chick nutrition. J. Sci. Food. Agr. 3: 43-48. Combs, G. F., and G. L. Romoser, 1955. A new approach to poultry feed formulation. Maryland Agr. Exp. Sta. Misc. Pub. No. 226. Combs, G. F., L. C. Norris and G. F. Heuser, 1942. The interrelationship of manganese, phosphatase and vitamin D in bone development. J. Nutrition, 23: 131-140. Common, R. H., T. J. Keefe, R. Burgess and W. A. Maw, 1950. Modification of biochemical responses of the immature pullet to estrogen by means of dietary aureomycin. Nature, 166: 992993. Cover, M. S., W. J. Mellen and E. Gill, 1955. Studies of hemorrhagic syndromes in chickens. Cornell Vet. 45:366-386. Dam, H., 1935a. The antihaemorrhagic vitamin of the chick. Occurrence and chemical nature. Nature, 135: 652-653. Dam, H., 1935b. The antihaemorrhagic vitamin of the chick. Biochem. J. 29: 1273-1285. Dam, H., J. Glavind, O. Bernth and E. Hagans, 1938. Anti-encephalomalacia activity of d-7tocopherol. Nature, 142:1157-1158. Dam, H., I. Kruse, I. Prange and E. Sjtadergaard, 1951. Substances affording a partial protection against certain vitamin E deficiency symptoms. Acta Physiol. Scand. 22: 299-310. Day, E. J., and J. E. Hill, 1957. The effect of calorieprotein ratio of the ration on growth and feed efficiency of turkeys. Poultry Sci. 36: 773-779. Delaplane, J. P., and J. H. Milliff, 1948. The grossand micro-pathology of sulfaquinoxaline poisoning in chickens. J. Am. Vet. Res. 9: 92.

Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 9, 2015

nicotinic acid. Poultry Sci. 32: 550-551. Beach, J. R., 1923. "Vitamin A" deficiency in poultry. Science, 58: 542. Beach, J. R., 1924. Studies on a nutritional deficiency of poultry caused by vitamin A deficiency. California Agr. Exp. Sta. Bui. 378. Bethke, R. M., and D. C. Kennard, 1924. Rearing chicks to maturity indoors. Poultry Sci. 4: 74-78. Bethke, R. M., P. R. Record and D. C. Kennard, 1931. A type of nutritional leg paralysis affecting chicks. Poultry Sci. 10: 355-368. Bethke, R. M., P. R. Record and D. C. Kennard, 1933. Relation of the vitamin G complex to hatchability and nutritive properties of eggs. Poultry Sci. 12:332-333. Biely, J., and B. March, 1951. The effect of aureomycin and vitamins on the growth rate of chicks. Science, 114: 330-331. Bird, F. H., 1950. The "animal protein factor" and mortality in chicks. Poultry Sci. 29: 314-315. Bird, H. R., R. J. Lillie and J. R. Sizemore, 1952. Environment and stimulation of chick growth by antibiotics. Poultry Sci. 31: 907. Black, S., R. S. Overman, C. A. Elvehjem and K. P. Rink, 1942. Effect of sulfaguanidine on rat growth and plasma prothrombin. J. Biol. Chem. 145: 137-143. Bornstein, S., and Y. Samberg, 1954. Field cases of vitamin K deficiency in Israel. Poultry Sci. 33: 831-836. Briggs, G. M., 1946. Nicotinic acid deficiency in turkey poults and the occurrence of perosis. J. Nutrition, 31: 79-84. Briggs, G. M., E. G. Hill and M. J. Giles, 1950. Vitamin B12 in all-plant rations for chicks and sparing activity of methionine and choline. Poultry Sci. 29: 723-736. Briggs, G. M., Jr., T. D. Luckey, L. J. Tepley, C. A. Elvehjem and E. B. Hart, 1943. Studies on nicotinic acid deficiency in the chick. J. Biol. Chem. 148: 517-522. Buckner, G. D., E. H. Nollau and J. H. Kastle, 1916. The feeding of young chickens on grain mixtures of high and low lysine content. Am. J. Physiol. 39: 162-171. Bunnell, R. H., L. D. Matterson, E. P. Singsen, L. M. Potter, A. Kozeff and E. L. Jungherr, 1955. Studies on encephalomalacia in the chick. 3. The influence of feeding or injecting various tocopherols and other antioxidants on the incidence of encephalomalacia. Poultry Sci. 34: 1068-1079. Caskey, C. D., and L. C. Norris. 1938. Further studies on the role of manganese in poultry nutrition. Poultry Sci. 17: 433. Caskey, C. D., W. D. Gallup and L. C. Norris, 1939.

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L. C. NORRIS the importance of managanese in the nutrition of poultry. Poultry Sci. 16: 351-352. Gallup, W. D., and L. C. Norris, 1938. The essentialness of manganese for the normal development of bone. Science, 87: 18-19. Gallup, W. D., and L. C. Norris, 1939. The effect of a deficiency of manganese in the diet of the hen. Poultry Sci. 18:83-88. Gillis, M. B., and L. C. Norris, 1949a. Effect of the animal protein factor on the requirement for methylating compounds. J. Biol. Chem. 179: 487-488. Gillis, M. B., and L. C. Norris, 1949b. Vitamin B i 2 and the requirement of the chick for methylating compounds. Poultry Sci. 28: 749-750. Goldhaft, T. M., and N. Wernicoff, 1954. A report on a haemorrhagic condition occurring in poultry in the United States. 10th World's Poultry Congress, p. 278. Gordon, R. F., 1951. Observations on an outbreak of disease in fowls possibly associated with sulphaquinoxaline poisoning. 9th World's Poultry Congress, Vol. I l l , p. 95-101. Grau, C. R., and M. Kamei, 1950. Amino acid imbalance and the growth requirements for lysine and methionine. J. Nutrition, 41: 89-101. Gray, J. E., G. H. Snoeyenbos and I. M. Reynolds, 1954. The hemorrhagic syndrome of chickens. J. Am. Vet. Med. Assoc. 125: 144-151. Grijns, G., 1901. Polyneuritis gallinarum. Geneeskundig. Tijdschrift Nederlandsch.-Indie 41: 3. Griminger, P., H. Fisher, W. D. Morrison, J. M. Snyder and H. M. Scott, 1953. Factors influencing blood clotting time in the chick. Science, 118: 379-380. Halpin, J. G., C. E. Holmes and E. B. Hart, 1933. Vitamin G inadequate in many rations for laying hens. Wisconsin Agr. Exp. Sta. Bui. 425: 18-19. Harned, B. K., R. W. Cunningham, M. C. Clark, R. Cosgrove, C. R. Hine, W. J. McCauley, E. Stokey, R. E. Vessey, N. N. Yaud and Y. SubbaRow, 1948. The pharmacology of duomycin (aureomycin). Ann. New York Acad. Sci. 51: 182-210. Hart, E. B., J. G. Halpin and H. Steenbock, 1917. The behavior of chickens restricted to the wheat or maize kernel. I I . J. Biol. Chem. 31: 415-420. Hart, E. B., J. G. Halpin and H. Steenbock 1920. Use of synthetic diets in the growth of baby chicks. A study of leg weakness in chickens. J.Biol. Chem. 43: 421-422. Hart E. B., J. G. Halpin and H. Steenbock, 1922. The nutritional requirement of baby chicks. I I . Further study of leg weakness in chickens. J. Biol. Chem. 52: 379-386.

Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 9, 2015

Donaldson, W. E., G. F. Combs and G. L. Romoser, 1956. Studies on energy levels in poultry rations. 1. The effect of calorie-protein ratio of the ration on growth, nutrient utilization and body composition of chicks. Poultry Sci. 35: 1100-1105. Drummond, J. C , 1916. Observations upon the growth of young chickens under laboratory conditions. Biochem. J. 10: 77-88. Drummond, J. C , 1920. The nomenclature of the so-called accessory food factors (vitamins). Biochem. J. 14: 660. Eijkman, C , 1897. Eine Beri-Beri-ahnliche Krankheit der Huhner. Archiv. Path. Anat. und Physiol. 148:523-532. Eijkman, C , 1906. tjber Ernahrungspolyneuritis. Archiv Hygiene, 58:150-170. Emmett, A. D., and G. E. Peacock, 1922. The chick as an experimental animal in vitamin studies. A preliminary report. J. Biol. Chem. 50: XL-XLI. Emmett, A. D., and G. Peacock, 1923. Does the chick require fat-soluble vitamins? J. Biol. Chem. 56: 679-693. Ferguson, T. M., H. P. Vaught, L. D. Matterson, B. L. Reid and J. R. Couch, 1957. The effect of different levels of productive energy, protein and methionine upon the growth of Broad Breasted Bronze turkey poults. Poultry Sci. 36:124-128. Fisher, H., and C. B. Hudson, 1956. Chick viability and pantothenic acid deficiency in the breeding diet. A case report. Poultry Sci. 35:487-488. Fraps, G. S., 1946. Composition and productive energy of poultry feeds and rations. Texas Agr. Exp. Sta. Bui. 678. Frost, D. V., and H. C. Spruth, 1955. Control of hemorrhagic condition in chickens with menadione sodium bisulfite. Poultry Sci. 34: 56-64. Funk, C , 1912. The etiology of the deficiency diseases. J. State Med. 20: 341-368. Funk, C , 1913. Studien uber das Wachstum. I. Mitteilung. Das Wachstum auf vitamin-haltiger und vitaminfreier Nahrung. Z. physiol. Chem. 88: 352-356. Funk, C , 1914. Studies on growth. The influence of diet on growth, normal and malignant. Lancet, I: 98-101. Funk, C , 1916. The study of the dietary conditions bearing on the problem of growth in rats. J. Biol. Chem. 27: 1-14. Funk, C , and A. B. Macallum, 1914. Die chemischen Determinaten des Wachstums. Z. physiol. Chem. 92: 13-20. Gallup, W. D., and L. C. Norris, 1937a. Studies on the perosis preventing properties of manganese. J. Biol. Chem. 117: XXXVI-XXXVII. Gallup, W. D., and L. C. Norris, 1937b. Studies on

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tenance and egg production. Poultry Sci. 24: 142-145. Hill, D. C , H. D. Branion and S. J. Slinger, 1952. Influence of environment on the growth response of chicks to penicillin. Poultry Sci. 31: 920. Hill, F. W., 1953. New information on lysine and methionine requirements of chicks. Proc. Cornell Nutr. Conf. for Feed Mfgrs., p. 44-60. Hill, F. W., and L. M. Dansky, 1954. Studies on the energy requirements of chickens. 1. The effect of dietary energy level on growth and feed consumption. Poultry Sci. 33: 112-119. Hill, F. W., and R. Renner, 1957. Metabolizable energy values of feedstuffs for poultry and their use in formulation of rations. Proc. Cornell Nutr. Conf. for Feed Mfgrs., p . 22-32. Hogan, A. G., L. R. Richardson, H. Patrick and H. L. Kempster, 1941. Perosis due to a vitamin deficiency. J. Nutrition, 21:327-340. Hogan, A. G., N. B. Guerrant and H. L. Kempster, 1925. Concerning the adequacy of synthetic diets for the growth of the chick. J. Biol. Chem. 64: 113-124. Hopkins, F. G., 1912. Feeding experiments illustrating the importance of accessory factors in normal dietaries. J. Physiol. 49: 425-450. Hunter, J. E., and E. M. Funk, 1930. The production of "slipped tendon" in chicks by experimental feeding. Proc. 22nd Ann. Mtg. Poultry Sci. Assn., p. 45-47. Jukes, T. H., 1939. The pantothenic acid requirement of the chick. J. Biol. Chem. 129: 225-231. Jukes, T. H., 1940a. Prevention of perosis by choline. J. Biol. Chem. 134: 789-790. Jukes, T. H., 1940b. Effect of choline and other supplements on perosis. J. Nutrition, 20: 445-458. Jukes, T. H., and E. L. R. Stokstad, 1952. Further observations on the utilization of homocystine, choline and related compounds by chicks. J. Nutrition, 48: 209-229. Jungherr, E. L., 1936. A field condition resembling nutritional encephalomalacia in chicks. Science, 84: 559-560. Kline, O. L., M. O. Schultze and E. B. Hart, 1932. Carotene and xanthophyll as sources of vitamin A for the growing chick. J. Biol. Chem. 97: 83-91. Lease, J. G., and H. T. Parsons, 1934. The relationship of dermatitis in chicks to lack of vitamin B2 and to dietary egg white. Biochem. J. 28: 21092115. Lepkovsky, S., and T. H. Jukes, 1935. Growth promoting effect of flavine on the chick. Science, 82:326. Lepkovsky, S., and T. H. Jukes, 1936. The response of rats, chicks and turkey poults to crystalline

Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 9, 2015

Hart, E. B., H. Steenbock, S. Lepkovsky and J. G. Halpin, 1923. The nutritional requirements of baby chicks. I I I . The relation of light to the growth of the chicken. J. Biol. Chem. 58: 33-41. Hart, E. B., H. Steenbock, S. Lepkovsky and J. G. Halpin, 1924. The nutritional requirements of baby chicks. IV. The chick's requirement for vitamin A. J. Biol. Chem. 60:341-354. Hart, E. B., H. Steenbock, S. Lepkovsky, W. F. Kletzien, J. G. Halpin and O. N. Johnson, 1925. The influence of ultraviolet light on the production, hatchability and fertility of eggs. J. Biol. Chem. 65: 579-595. Hauge, S. M., C. W. Carrick and R. W. Prange, 1927. Fat soluble A requirements for growing chicks. Poultry Sci. 6: 135-140. Hayward, J. W., and F. H. Hafner, 1941. The supplementary effect of cystine and methionine upon the protein of raw and cooked soybeans as determined with chicks and rats. Poultry Sci. 20: 139-149. Hayward, J. W., J. G. Halpin, C. E. Holmes, G. Bohstedt and E. B. Hart, 1937. Soybean oil meal prepared at different temperatures as a feed for poultry. Poultry Sci. 16:3-14. Hegsted, D. M., J. J. Oleson, R. C. Mills, C. A. Elvehjem and E. B. Hart, 1940. Studies on a dermatitis in chicks distinct from pantothenic acid deficiency. J. Nutrition, 20: 599-606. Hegsted, D. M., R. C. Mills, C. A. Elvehjem and E. B. Hart, 1941. Choline in the nutrition of chicks. J. Biol. Chem. 138:459-466. Heiman, V., 1935. The relative vitamin G content of dried whey and dried skimmilk. Poultry Sci. 14: 137-146. Heiman, V., and L. C. Norris, 1933. The relative vitamin G content of milk sugar feed (dried whey) and dried skimmilk. Poultry Sci. 12: 332. Heiman, V., R. A. Sullivan and L. C. Norris, 1934. Evidence that lactochrome is one factor of the vitamin G complex. Cornell Univ. Agr. Exp. Sta. 49th Ann. Rept.: 118-119. Heller, V. G., and R. Penquite, 1937. Factors producing and preventing perosis in chickens. Poultry Sci. 16: 243-246. Heuser, G. F., and F. V. Kosikowsky, 1952. Effect of procaine penicillin on pH of contents of small intestine. Unpublished results, Cornell Univ. Agr. Exp. Sta. Heuser, G. F., and L. C. Norris, 1952. Some results of feeding antibiotics to chickens. Poultry Sci. 31: 857-862. Heuser, G. F., L. C. Norris, H. T. Peeler and M. L. Scott, 1945. Further studies on the apparent effect of digestibility upon growth, weight main-

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272

L. C. NORRIS The vitamin requirements of growing chickens. Poultry Sci. 2:117-124. Moore, P. R., A. Evenson, T. D. Luckey, E. McCoy, C. A. Elvehjem and E. B. Hart, 1946. Use of sulfasuxidine, streptothricin and streptomycin in nutritional studies with the chick. J. Biol. Chem. 165: 437-441. Nelson, T. S., and L. C. Norris. 1956. Studies on the relation of vitamin K deficiency to the field hemorrhagic syndrome. Poultry Sci. 35: 1162. Nelson, T. S., L. C. Norris, F. W. Hill, M. L. Scott and G. F. Heuser, 1957. Further studies on the requirement of chicks for methionine and cystine. Proc. Cornell Nutr. Conf. for Feed Mfgrs., p. 126-131. Norris, L. C , and C. D. Caskey, 1939. A chronic congenital ataxia and osteodystrophy in chicks due to manganese deficiency. J. Nutrition, 17: (Proc.) 16-17. Norris, L. C , and T. S. Nelson, 1955. The hemorrhagic syndrome of the chick. Proc. AFMA Nutr. Counc, Nov. 27-29, p. 17-20. Norris, L. C , and A. T. Ringrose, 1935. The requirement of poultry for vitamin G. Cornell Univ. Agr. Exp. Sta., 48th Ann. R e p t : 129. Norris, L. C , H. J. Davis, and R. C. Sullivan, 1935. The role of flavin in the nutrition of poultry. Cornell Univ. Agr. Exp. Sta. 48th Ann. Rept.: 132-133. Norris, L. C , G. F. Heuser and H. S. Wilgus Jr., 1930. Is the chief value of milk for feeding poultry due to the presence of a new vitamin? Poultry Sci. 9: 133-140. Norris, L. C , G. F. Heuser, H. S. Wilgus, Jr. and A. T. Ringrose, 1931. The occurrence in chicks of a paralysis of nutritive origin. Poultry Sci. 10: 93-97. Norris, L. C , H. S. Wilgus, Jr., A. T. Ringrose, V. Heiman and G. F. Heuser, 1936. The vitamin G requirement of poultry. Cornell Univ. Agr. Exp. Sta. Bui. 660. Oleson, J. J., B. L. Hutchings and A. R. Whitehill, 1950. The effect of feeding aureomycin on the vitamin B12 requirement of the chick. Arch. Biochem. 29: 334-338. Osborne, T. B., and L. B. Mendel, 1913. The influence of butter-fat on growth. J. Biol. Chem. 16: 423-437. Osborne, T. B., and L. B. Mendel, 1914. The influence of cod liver oil and some other fats on growth. J. Biol. Chem. 17: 401-408. Osborne, T. B., and L. B. Mendel, 1916. The effect of the amino acid content of the diet on the growth of chickens. J. Biol. Chem. 26: 293-300. Osborne, T. B., and L. B. Mendel, 1918. The growth

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vitamin G (flavin). J. Nutrition, 12: 515-526. Lillie, R. J., C. A. Denton and H. R. Bird, 1948. Relation of vitamin B12 to the growth factor present in cow manure. J. Biol. Chem. 176: 1477. Lillie, R. J., M. W. Olsen and H. R. Bird, 1949. Role of vitamin B12 in reproduction in poultry. Proc. Soc. Exp. Biol. Med. 72: 598-602. Lindblad, G. S., S. J. Slinger, G. W. Anderson and I. Motzok, 1952. Effect of aureomycin on the calcium and phosphorus requirements of chicks. Poultry Sci. 31:923-924. Lyons, M., and W. M. Insko, Jr., 1937. Chondrodystrophy in the chick embryo produced by manganese deficiency in the diet of the hen. Kentucky Agr. Exp. Sta. Bull. 371. Matterson, L. D., and E. P. Singsen, 1951. A comparison of several antibiotics as growth stimulants in practical chick starting rations. Storrs Agr. Exp. Sta. Bull. 275. McCollum, E. V., and M. Davis, 1913. The necessity of certain lipins in the diet during growth. J. Biol. Chem. 15: 167-175. McCollum, E. V., and C. Kennedy, 1916. The dietary factors operating in the production of polyneuritis. J. Biol. Chem. 24: 491-502. McCollum, E. V., N. Simonds, J. E. Backer and P. G. Shipley, 1922. Studies on experimental rickets. XXI. An experimental demonstration of the existence of a vitamin which promotes calcium deposition. J. Biol. Chem. 53: 293-312. McGinnis, J., P. T. Hsu and W. D. Graham, 1948. Studies on an unidentified factor required by chicks for growth and protein utilization. Poultry Sci. 27: 674-675. McGinnis, J., L. C. Norris and G. F. Heuser, 1942. Effect of ethanolamine and betaine on perosis in chicks. Proc. Soc. Exp. Biol. Med. 51: 293-294. McGinnis, J., L. C. Norris and G. F. Heuser, 1944. Influence of diet on chick growth promoting and antiperotic properties of betaine, methionine and choline. Proc. Soc. Exp. Biol. Med. 56: 197-200. Migicovsky, B. B., A. M. Nielson, M. Gluck and R. Burgess, 1951. Penicillin and calcium absorption. Arch. Bioch. Biophys. 34: 479-480. Miller, E. C , M. L. Sunde and C. A. Elvehjem, 1957. Minimum protein requirements of laying pullets at different energy levels. Poultry Sci. 36: 681-690. Miller, R. F., L. C. Norris and G. F. Heuser, 1956. The vitamin B12 requirement of White Leghorn chicks. Poultry Sci. 35: 342-349. Milligan, J. L., G. H. Arscott and G. F. Combs, 1952. Vitamin B12 requirement of New Hampshires. 2. Influence of maternal ration on requirement of progeny. Poultry Sci. 31: 830-837. Mitchell, H. H., F. E. Kendall and L. E. Card, 1923.

FIFTY YEARS IN POULTRY NUTRITION

1948. The relation of energy to fiber in chick rations. Poultry Sci. 27: 736-741. Ross, E., and H. Yacowitz, 1952. The effect of penicillin on vitamin D requirements for growth and bone calcification. Poultry Sci. 31: 933. Rubin, M., and H. R. Bird, 1947. A chick growth factor in cow manure. V. Relation to quantity and quality of soybean oil meal in the diet. J. Nutrition, 34: 233-245. Schaefer, A. E., W. D. Salmon and D. R. Strength, 1949. Interrelationship of vitamin B12 and choline. I. Effect on the growth of the chick. Proc. Soc. Exp. Biol. Med. 71: 202-204. Schonheyder, F., 1935. The antihaemorrhagic vitamin of the chick. Measurement and biological action. Nature, 135: 653. Scott, H. M., L. D. Matterson and E. P. Singsen, 1947. Nutritional factors influencing growth and efficiency of feed utilization. 1. The effect of the source of carbohydrate. Poultry Sci. 26: 554. Scott, M. L., 1951. Studies on the enlarged hock disorder in turkeys. 3. Evidence of the detrimental effect of fish liver oil and the beneficial effect of dried brewers yeast and other materials. Poultry Sci. 30: 846-855. Scott, M. L., 1953. Prevention of the enlarged hock disorder in turkeys with niacin and vitamin E. Poultry Sci. 32:670-677.' Scott, M. L., and G. F. Heuser, 1952. Studies in duck nutrition. 4. Bowed legs in ducks caused by niacin deficiency. Poultry Sci. 31: 752. Scott, M. L., G. F. Heuser and L. C. Norris, 1948. Energy, protein and unidentified vitamins in poult nutrition. Poultry Sci. 27: 773-780. Shelton, D. C , G. C. Anderson, J. K. Bletner, C. E. Weakley, Jr., R. C. Cook and W. R. Lewis, 1954. The role of coccidiostats and growth stimulators in the chick hemorrhagic condition. Poultry Sci. 33: 1080. Sherwood, R. M., and J. R. Couch, 1936. Wheat gray shorts for the prevention of slipped tendons in battery brooder chicks. Texas Agr. Exp. Sta. Bui. 525. Sherwood, R. M., and G. S. Fraps, 1936. Constituents of wheat gray shorts which prevent slipped tendon. Poultry Sci. 15: 424. Singsen, E. P., R. H. Bunnell, L. D. Matterson, A. Kozeff and E. L. Jungherr, 1955. Studies on encephalomalacia in the chick. 2. The protective action of diphenyl-p-phenylene diamine against encephalomalacia. Poultry Sci. 34: 262-271. Singsen, E. P., L. D . Matterson and A. Kozeff, 1950. The effect of sources of carbohydrate on the feeding efficiency of laying hens. Poultry Sci. 29: 779-780. Singsen, E. P., L. D. Matterson, A. Kozeff, R. H.

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of chickens in confinement. J. Biol. Chem. 33: 433-438. Ott, W. H., E. L. Rickes and T. R. Wood, 1948. Activity of crystalline vitamin B12 for chick growth. J. Biol. Chem. 174: 1047-1048. Panda, J. N., and G. F. Combs, 1950. Studies on the energy requirement of the chick for rapid growth. Poultry Sci. 29: 774-775. Pappenheimer, A. M., and M. Goettsch, 1931. A cerebellar disorder in chicks apparently of nutritional origin. J. Exp. Med. 53: 11-26. Pappenheimer, A. M., and M. Goettsch, 1934. Protection afforded by certain vegetable oils against nutritional encephalomalacia of chicks. Proc. Soc. Exp. Biol. Med. 31: 777-779. Patterson, E. B., J. R. Hunt, P. Vohra, L. G. Blaylock and J. McGinnis, 1956. The niacin and tryptophan requirements of chicks. Poultry Sci. 35:499-504. Payne, L. F., J. S. Hughes and H. F. Leinhardt, 1932. The etiological factors involved in the malformation of bones in young chickens. Poultry Sci. 11: 158-165. Peeler, H. T., R. F. Miller, C. W. Carlson, L. C. Norris and G. F. Heuser, 1951. Studies of the effect of vitamin B12 on hatchability. Poultry Sci. 30: 11-17. Pepper, W. F., S. J. Slinger and I. Motzok, 1951. The effect of aureomycin on the interrelationship between manganese and salt in chicks. Poultry Sci. 30:926-927. Petersen, C. F., A. C. Wiese, C. E. Lampman and R. V. Dahlstrom, 1950. Role of crystalline vitamin B12 for hatchability. Poultry Sci. 29:618-619. Reynolds, W. M., W. K. Warden and H. G. Luther, 1953-1954. Antibiotics, vitamin K and blood clotting time in poultry. Antibiotics Ann., p. 380-385. Rickes, E. L., N. G. Brink, F. R. Koniuszy, T. R. Wood and K. Folkers, 1948. Crystalline vitamin B12. Science, 107: 396-397. Ringrose, A. T., and L. C. Norris, 1934. The complex nature of vitamin G. Cornell Univ. Agr. Exp. Sta., 47th Ann. Rept., p. 120-121. Ringrose, A. T., and L. C. Norris, 1936a. Differentiation between vitamin G and an insoluble factor preventing a pellagra-like syndrome in chicks. I. J. Nutrition, 12: 535-552. Ringrose, A. T., and L. C. Norris, 1936b. Differentiation between vitamin G and a soluble factor preventing a pellagra-like syndrome in chicks. I I . J. Nutrition, 12: 552-569. Ringrose, A. T., L. C. Norris and G. F. Heuser, 1931. The occurrence of a pellagra-like syndrome in chicks. Poultry Sci. 10: 166-177. Robertson, E. I., R. F. Miller and G. F. Heuser,

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L. C. NORRIS Poultry Sci. 31: 621-627. Whitehill, A. R., J. J. Oleson and B. L. Hutchings, 1950. Stimulatory effect of aureomycin on the growth of chicks. Proc. Soc. Exp. Biol. Med. 74: 11-13. Wiese, A. C , G. H. Benham, C. A. Elvehjem and E. B. Hart, 1941. Further bone phosphatase studies in chick perosis. Poultry Sci. 20: 255-258. Wiese, A. C , B. C. Johnson, C. A. Elvehjem, E. B. Hart and J. G. Halpin, 1939. A study of blood and bone phosphatase in chick perosis. J. Biol. Chem. 127:411-420. Wilgus, H. S., Jr., L. C. Norris and G. F. Heuser, 1935. The relative protein efficiency and the relative vitamin G content of common protein supplements used in poultry rations. J. Agr. Res. 51:383-399. Wilgus, H. S., Jr., L. C. Norris and G. F. Heuser, 1936a. The role of certain inorganic elements in the cause and prevention of perosis. Science, 84: 252-253. Wilgus, H. S., Jr., L. C. Norris and G. F. Heuser, 1936b. Effect of heat on the nutritive value of soybean oil meal. Ind. Eng. Chem. 28: 586-588. Wilgus, H. S., Jr., L. C. Norris and G. F. Heuser, 1937. The role of manganese and certain other trace elements in the prevention of perosis. J. Nutrition, 14: 155-167. Williams, R. G., J. H. Truesdail, H. H. Weinstock, Jr., E. Rhorman, C. M. Lyman and C. H. McBurney, 1938. Pantothenic acid. II. Its concentration and purification from liver. J. Am. Chem. Soc. 60: 2719-2723. Yacowitz, H., R. D. Carter and E. Ross, 1955. Further studies on hemorrhagic syndrome induced by feeding high levels of sulfaquinoxaline to chicks. Poultry Sci. 34: 1229. Yacowitz, H., L. C. Norris and G. F. Heuser, 1951. Evidence for an interrelationship between vitamin Bi2and pantothenic acid. J. Biol. Chem. 192: 141-146. Yacowitz, H., R. F. Miller, L. C. Norris and G. F. Heuser, 1952. Vitamin B12 studies with the hen. Poultry Sci. 31: 89-98. Young, R. J., L. C. Norris and G. F. Heuser, 1954. The utilization by vitamin Bi2-deficient chicks of monomethylaminoethanol, homocystine and betaine as precursors of choline and homocystine. J. Nutrition, 53: 233-248.

MAY 21-23. AMERICAN FEED MANUFACTURERS' ASSOCIATION, MORRISON HOTEL, CHICAGO, ILLINOIS JUNE 24-27. NATIONAL PLANS CONFERENCE, KENTUCKY^HOTEL, LOUISVILLE, KENTUCKY

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Bunnell and E. L. Jungherr, 1954. Studies on encephalomalacia in the chick. 1. The influence of a vitamin E deficiency on the performance of breeding hens and their chicks. Poultry ScL 33: 192-201. Steenbock, H., and P. W. Boutwell, 1920. Fatsoluble vitamine. III. The comparative nutritive value of white and yellow maizes. J. Biol. Chem. 41:81-96. Stekol, J. A., P. T. Hsu, S. Weiss and P. Smith, 1953. Labile methyl group and its synthesis de novo in relation to growth in chicks. J. Biol. Chem. 203: 763-773. Stokstad, E. L. R., and T. H. Jukes, 1950. Further observations on the "animal protein factor." Proc, Soc. Exp. Biol. Med. 73: 523-528. Stokstad, E. L. R., and T. H. Jukes, 1951. Effect of various levels of vitamin Bi2 upon growth response produced by aureomycin in chicks. Proc. Soc. Exp. Biol. Med. 76: 73-76. Stokstad, E. L. R., T. H. Jukes, J. Pierce, A. C. Page, Jr. and A. L. Franklin, 1949. The multiple nature of the animal protein factor. J. Biol. Chem. 180: 647-654. Sunde, M. L., 1953. The niacin requirement of chickens from 6 to 11 weeks of age. Poultry Sci. 32: 926. Sunde, M. L., 1956. A relationship between protein level and energy level in chick rations. Poultry Sci. 35:350-354. Sweet, G. B., G. L. Romoser and G. F. Combs, 1954. Further observations on the effect of sulfaquinoxaline, p-aminophenylarsonic acid and oxytetracycline on blood clotting time of chicks. Poultry Sci. 33:430-432. Titus, H. W., 1932. Perosis, or deforming leg weakness in the chicken. Poultry Sci. 11:117-125. Titus, H. W., and W. M. Ginn, 1931. Rice bran a preventive of perosis (deforming leg weakness) in chickens. Science, 74: 249-250. van der Hoorn, R., H. D. Branion and W. R. Graham, Jr., 1938. Studies in the nutrition of the chick. III. A maintenance factor present in wheat germ and the effect of the addition of a small amount of manganese dioxide to the diet. Poultry Sci. 17:185-192. Waibel, P. E., M. L. Sunde and W. W. Cravens, 1952. Effect of addition of penicillin to the hen's ration on biotin and folic acid content of eggs.