RESEARCH PAPERS. Possible Role of Beta-Carotene in Improving Fertility in Dairy Cattle 1,2

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1 RESEARCH PAPERS Possible Role of Beta-Carotene in Improving Fertility in Dairy Cattle 1,2 R. W. HEMKEN and D. H. BREMEL Animal Science Department University of Kentucky Lexington ABSTRACT Recent interest in /3-carotene has been stimulated by reports that reproductive performance in cattle was improved with dietary supplementation of /3-carotene even when the diet was supplemented with vitamin A. Vitamin A requirements for cattle are based on studies with /3- carotene as the vitamin A source and with studies with vitamin A in the ester or alcohol form. Most of the studies with cattle that demonstrate the need for vitamin A for optimum reproduction were when /3-carotene was the source of vitamin A. Recent German reports show an improvement in conception rate, intensity of estrus, and changes in luteinizing hormone patterns when cattle received /3-carotene supplementation of low carotene diets. These diets were supplemented with vitamin A. A similar study from Israel did not detect benefits of/3- carotene. The active form of vitamin A for reproduction in rats and other species has not been determined; however, vitamin A does meet the reproductive requirements. The ruminant animal does have differences in carotene metabolism from the rat. Before the role of/3-carotene for reproduction in cattle can be clarified, the specific function of carotene or the specific form of vitamin A for reproduction needs to be determined. Received October 19, Invitational paper presented at the 76th Annual Meeting of the American Dairy Science Association, June 29, This manuscript ( ) is published with the approval of the Director of Kentucky Agricultural Experiment Station. DISCUSSION Recent publications from Germany (1, 20, 21, 22, 25, 31, 32) have stimulated a renewed interest in /3-carotene for ruminant animals. They reported improved reproductive performance for cattle supplemented with /J-carotene even when the diet was supplemented with vitamin A. Prior to these reports, it was assumed that vitamin A fed adequately as retinyl esters would eliminate reproductive problems associated with this vitamin. These reports suggest a requirement for /3-carotene that cannot be met as supplemental A. Vitamin A has been established as essential for vision, growth, reproduction, and maintenance of differentiated epithelia and of mucous secretion. The main emphasis of this review will be concerned with the role of/3- carotene and vitamin A for reproduction. Other aspects of vitamin A metabolism will be discussed to show the need for clarification of vitamin metabolism before the role of /3- carotene for optimum reproduction can be established. Carotene Requirements for Dairy Cattle A number of criteria have been used to establish the carotene and vitamin A requirement for dairy cattle, and the minimum amount of carotene required by these different measurements varies considerably. Eaton et al. (5) concluded that 29/lg (96.7 IU) of vitamin A/kg of live weight was needed to prevent elevated cisteral cerebrospinal fluid pressures (68 mm of saline) for calves. In the calf, the elevated cerebrospinal fluid pressure is apparently the earliest change specific for vitamin A deficiency. The same group (6) reported that 106/~g of carotene/kg body weight was needed to prevent elevated cerebrospinal fluid pressure. Similar studies (26, 27, 31) with carotene indi J Dairy Sci. 65:

2 1070 HEMKEN AND BREMEL cated a requirement of 66 to 73 #g/kg required to maintain normal cerebrospinal fluid pressure below 120 mm of saline. The amount of carotene required to prevent night blindness (14, 28) and obtain normal growth (13) is less than half the amount required to prevent elevated cerebrospinal fluid pressure. When carotene required to prevent papillary edema was studied (27, 31, 37), the results were variable and ranged from 24 to 79/.tg/kg of body weight. Several estimates (4, 19, 30) of the amount of carotene required to maintain normal reproduction indicate a higher requirement (60 to 198/ag/kg) than those reported for other functions. However, the numbers of animals used and the accuracy of these estimates could be questioned. The high amount was for Guernsey cattle. Other measures used to establish carotene requirements included the amount needed to maintain plasma carotene, plasma vitamin A, or liver storage of vitamin A at a specified concentration. Results of estimates based on liver and plasma concentrations are dependent on the concentration selected. Estimates (7, 13) of carotene required to increase liver content of vitamin A are higher (125 and 132 /ag/kg of body weight) than those for maintenance of plasma or liver concentrations. Current US recommendations by the National Research Council (29) are higher than the amount of vitamin A considered minimal by Eaton et al. (5) and do not specify any specific carotene requirement. Requirements are listed as the international units of vitamin A required and 1 mg of carotene is considered equivalent to 400 IU of vitamin A. Reproductive Problems That some form of vitamin A is essential for reproduction is established for cattle as well as for other species. The literature published prior to 1950 was concerned primarily with carotene, whereas greater emphasis was given to vitamin A during the next 20 yr. The recent interest in the role of/3-carotene has revived an interest in the vitamin A precursor. A report by Hart and Guilbert (15) in 1933 described a number of reproductive problems associated with a low intake of vitamin A or its precursor. Symptoms of deficiency included birth of dead or weak calves, a high incidence of retained placenta, and some abortions. The COWS also had night blindness, opthalmia, and diarrhea. Kuhlman and Gallup (19) reported lowered conception rates for cattle fed 44 compared with 84 /.tg carotene per kg body weight; however, the differences probably would not be statistically different. Asdell (2), in a review, discussed a report by Axelsson in 1947 in which cattle fed diets containing 27 to 47 mg of carotene had 2.0 services per conception as compared with 1.4 services per conception of cattle fed 48 to 72 mg of carotene. Study of reproduction in bulls fed vitamin A deficient diets (8, 16, 34) indicated that other gross symptoms of deficiency occurred prior to reproductive failure. However, deficiency did delay puberty and reduce libido and spermatogenesis. Lotthammer (20), in reviewing the recent German studies on the importance of/3-carotene for fertility of cattle, gave two reasons for their interest. Several studies showed a high concentration of/6-carotene in the ovaries, with the corpus luteum containing a high concentration of /3-carotene and no vitamin A. Other studies had related low 13-carotene content of the feed or blood with lowered fertility. In a series of five papers (1, 22, 25, 27, 32), involving a number of experiments, reproduction was examined with heifers of the German Black Pied breed. The basic ration was old, low-13-carotene hay. The control ration was supplemented with vitamin A (220 IU/kg body weight), and the treatment group included supplemental.3 mg/~-carotene plus 100 IU of supplemental vitamin A per kg body weight. They did not specify the form of the vitamin A supplement. In the first report from this series, Meyer et ~l. (25) reported a significant increase in the interval between estrous periods, 20.4 and 20.9 versus 19.6 and 20.2 days for two trials for the carotene supplemental and control groups. In addition, the length of the estrous period was longer for the carotene-deficient groups (2.4 and 2.9 versus 1.9 and 2.2 days). These estrous periods are longer than most reports but are based on rectal palpations as well as visual observations. Other differences included increased time (about 1 day) between beginning of estrus and ovulation time, reduced uterine contraction, and estrol follicles were firmer on the first day of estrus and the corpus luteum was smaller for the low-carotene group.

3 BETA-CAROTENE FOR FERTILITY: REVIEW 1071 In a second paper about the same heifers, Lotthammer et al. (23) described other reproductive characteristics. Conception rate was reduced for heifers fed the low-carotene diet as the number of inseminations per conception was 2.00 as compared with 1.42 for the carotene-supplemented diet. Other results indicated a lower intensity of estrus and a higher frequency of corpora lutea and/or luteal cysts for the low-carotene groups. The third (21) and fourth (32) papers in this series investigated blood serum nutrient and hormonal measures. The only nutrient related to ovarian function was blood serum /3-carotene. Hormone functions altered by carotene content of the diet were a decrease in luteinizing hormone (LH) peak and a decreased interval from LH peak to ovulation for the/3-carotene supplemented heifers. Progesterone was not altered. Vitamin A was not related to hormonal functions; however, only total vitamin A was measured. The fifth paper (1) in the series compared tissue storage of vitamin A and /3-carotene, progesterone in the corpora lutea, and concentration of glucose and minerals in the uterine fluids. /3-carotene in liver and fat tissues was directly related to carotene intake and fertility. The concentration of progesterone in the corpora lutea was lower for the unsupplemented group. Lotthammer et al. (23) also reported on an experiment with older cows of the same breed which were started on low-/3-carotene diets 7 wk prior to parturition. The major effect on reproductive performance was an increase in embryonic mortality and early abortions for cows fed low-carotene rations. Blood and milk progesterone were lower for cows with interrupted pregnancy. In contrast to the German studies, Folman et al. (10) reported essentially negative results of a similar trial with Israeli-Friesian heifers maintained on a low-carotene diet starting at an average age of 7 mo. Carotene was supplemented at.3 mg/3-carotene/kg of body weight, and vitamin A was supplemented at 30/~g of retinal activity/kg body weight. They reported no differences in conception rate, duration of estrus, length of estrous cycle, plasma progesterone and LH concentrations, and interval between LH peak and ovulation. They suggested that the difference between this study and the German reports might be related to method of estrous detection and differences in insemination practice. Estrus was detected by a teaser bull, and each animal was inseminated twice at a 12-h interval in the study of Folrnan et al. (10). They did note a difference in growth rate in favor of the carotene-supplemented group. In addition to these controlled studies, several field studies (3, 11, 33) have reported improvement in conception rate or reduced days open for cows fed supplemental /3-carotene. In some field trials, no vitamin A supplementation was used, which would not eliminate low-vitamin A as the cause. Our interest in /3-carotene at Kentucky was stimulated by results of a low pregnancy rate (24%) for a group of heifers fed a low-carotene diet (17). Functions of Vitamin A and Carotene Prior to the German studies (20), there have been no reports of a specific function for /3- carotene. The active form of vitamin A for vision is retinal. However, the active form for growth, reproduction, and the maintenance of epithelial tissue has not been defined for any species (12). Results of feeding different forms of vitamin A indicate that the active form could be different for different functions. Retinoic acid maintained a normal growth rate and general health for rats; however, the rats were both blind and sterile. To complicate the picture further, the biological availability of /3-carotene to the ruminant animal has not been as clearly defined as it has been for the rat (9, 12, 36). Whereas ratsconvert carotene injected into the blood to vitamin A, Kon et al. (18) concluded that their studies provided virtually no evidence that carotene injected was converted to vitamin A in the calf. Many factors, both nutritional as well as environmental, can influence the vitamin A utilization and requirement. Ullrey (36) reviewed the biological availability of vitamin A and carotene and emphasized the need to understand the precise and specific structure and steriochemistry. He discussed the activity of the various carotenoid isomers and the relative amounts in some feeds. Corn is relatively high in isomers, which have a low activity. This may explain why some of the field problems have Journal of Dairy Science Vol. 65, No. 7, I982

4 1072 HEMKEN AND BREMEL been associated with corn silage feeding programs. Vitamin A given orally is hydrolyzed in the intestine, and the resulting retinol then is absorbed into the mucosal cell (36). This retinol is reesterified, and the retinyl esters are absorbed into the blood in association with lymph chylomicrons. The liver further converts this into primarily retinyl palmitate and stores it in the ester form. The vitamin A is mobilized from the liver as the free alcohol (retinol), and it is bound to plasma transport protein. The specificity of different tissues for one of the forms of vitamin A is demonstrated by the study of Tomlinson et al. (35). They demonstrated that vitamin A alcohol injected intravenously into dairy cows appeared in milk primarily in the ester form. Injected vitamin A palmitate had no measurable effect on concentration of vitamin A in milk. Plasma content of vitamin A was not related to reproductive performance in the German studies (1). However, they measured total vitamin and did not measure the various forms of vitamin A. Oral doses of vitamin A ester increase the ester form in the blood more than the alcohol form (24). Before a specific form of vitamin A is eliminated as the/3-carotene factor in reproduction, the forms of vitamin A available should be studied. If /3-carotene is a specific requirement for reproduction in the bovine, this would be a unique difference between the bovine and the rat. Further proof that /3-carotene is a specific requirement could be supported with injections of fl-carotene into problem reproductive animals if previous reports of essentially no conversion of/3-carotene post absorption by ruminants (19) is correct. Some knowledge of the active form of vitamin A for functions other than vision should give information that would allow evaluation of fl-carotene as a specific requirement. REFERENCES 1 Ahlswede, L., and K. H. Lotthammer. Untersuchungen uber eine spezifische Vitamin A-unahhangige Wirkung des /3-Carotins auf die Fertilitat des Rindes. 5. Mitt.: Organuntersuchungen -- Gewichtsund Gehaltsbestimmungen. Dtsch. Tierarztl. Wochenschr, 85: 7. 2 Asdell, A. S Nutrition and the treatment of sterility in dairy cattle: a review. J. Dairy Sci. 32: Cooke, P. C A study on the relationship between beta-carotene and fertility problems in dairy cows. Proc. Roche Syrup. Importance of Beta- Carotene for Bovine Fertil., London. 4 Davis, R. E., and L. L. Madsen Carotene and vitamin A in cattle blood plasma with observations on reproductive performance at restricted levels Of carotene intake. J. Nutr. 21: Eaton, H. D., J. E. Rousseau, Jr., R. C. Hall, Jr., H. I. Freir, and J. J. Lucas Reevaluation of the minimum vitamin A requirement of Holstein male calves based upon elevated cerebrospinal fluid pressure. J. Dairy Sci. 55: Eaton, H. D., J. E. Rousseau, Jr., G. G. Woelfel, M. C. Calhoun, S. W. Nielsen, and J. J. Lucas A reevaluation of the minimum carotene requirement of Holstein male calves based upon elevated cerebrospinal fluid pressure. Univ. Connecticut Coll. Agric. Exp. Sm. Bull Elliott, R. F Carotene requirements for young dairy calves. J. Dairy Sci. 32: Erh, R. E., F. N. Andrews, S. M. Hauge, and W. A. King Observations on vitamin A deficiency in young dairy bulls. J. Dairy Sci. 30: Fernandez, S. C., P. Buclowski, I. Ascarelli, H. Newark, and A. Bondi Preqntestinal stability of/3-carotene in ruminants. Int. J. Vitam. Nutr. Res. 46: Folman, Y., I. Ascarelli, Z. Herz, M. Rosenberg, M. Davidson, and A. Halevi Fertility of dairy heifers given a commercial diet free of /3- carotene. Br. J. Nutr. 41: Friesecke, H The significance of betacarotene in ruminant nutrition: field results - Europe. Proc. Roche Symp. Importance of Beta- Carotene for Bovine Fertil., London. 12 Goodman, D. S Vitamin A metabolism. Fed. Proc. 39: Guilbert, H. R., C. E. Howell, and G. H. Hart Minimum vitamin A and carotene requirements of mammalian species. J. Nutr. 19: Guilbert, H. R., and G. H. Hart Minimum vitamin A requirements with particular reference to cattle. J. Nutr. 10: Hart, G. H., and H. R. Guilbert Vitamin A deficiency as related to reproduction in range cattle. California Agric. Exp. Sm. Bull Hodgson, R. E., S. R. Hall, W. J. Sweetman, H. G. Wiseman, and H. T. Converse The effect of vitamin A deficiency on reproduction in dairy bulls. J. Dairy Sci. 29: Hurley, W. L The effect of dietary phosphorus level on reproduction in dairy heifers: effects on estrus behavior, and serum inorganic phosphorus, calcium, luteinizing hormone, progesterone, and estradiol. Ph.D. thesis, Univ. of Kentucky, Lexington. 18 Kon, S. K., W. A. McGillivray, and S. Y. Thompson Metabolism of carotene and vitamin A given by mouth or vein in oily solution or aqueous dispersion to calves, rabbits and rats. Br. J. Nutr. 9: Kuhlman, A. H., and W. D. Gallup Carotene

5 BETA-CAROTENE FOR FERTILITY: REV IEW (provitamin A) requirements of dairy cattle for conception. J. Dairy Sci. 25: Lotthammer, K. H Importance of /3-carotene for the fertility of dairy cattle. Feedstuffs 51:6. 21 Lotthammer, K. H., and L. Ahlswede Untersuchungen uber eine spezifische Vitamin A-unabhangige Wirkung des /3-Carotins auf die Fertilitat des Rindes. 3. Mitt.: Blutserumuntersuchungen. Dtsch. Tieraerztl. Wochenschr. 84: Lotthammer, K. H., L. Ahlswede, and H. Meyer Untersuchungen uber eine spezifische Vitamin A-unabhangige Wirkung des/3-carotins auf die Fertilitat des Rindes. 2. Mitt.: Weitere klinische Befunde und Besamungsergebnisse. Dtsch. Tieraerztl. Wochenschr. 83: Lotthammer, K. H., D. Schams, and H. Scholz Untersuchungen uber eine spezifische Vitamin A-unabhangige Wirkung des/3-carotene auf die Fruchtbarkeit von laktierended Kuhen. Zuchthygiene 13: McGillivray, W. A Factors influencing the vitamin content of milk fat. J. Dairy Res. 24: Meyer, J., L. Ahlswede, and K. H. Lotthammer Untersuchungen uber eine spezifische Vitamin A-unabhangige Wirkung des ~-Carotins auf die Fertilitat des Rindes. 1. Mitt.: Versuchsanstellung, Korperentwicklung und Eierstocksfunktion. Dtsch. Tieraerztl. Wochenschr. 82: Moore, L. A., J. F. Sykes, W. C. Jacobson, and H. G. Wiseman Carotene requirements for Guernsey and Jersey calves as determined by spinal fluid pressure. J. Dairy Sci. 31: Moore, L. A., H. M. Berry, and J. F. Sykes Carotene requirements for the maintenance of a normal spinal fluid pressure in dairy calves. J. Nutr. 26: Moore, L. A Carotene intake, level of blood plasma carotene and the development of papillary edema and nyctalopia in calves. J. Dairy Sci. 22: National Research Council Nutrient requirements of dairy cattle. 5th rev. ed. Natl. Acad. Sci., Washington, DC. 30 Ronning, M., E. R. Berousek, J. R. Griffith, and W. D. Gallup Carotene requirements of dairy cattle. Oklahoma Agric. Exp. Stn. Tech. Bull. T Rousseau, J. E., Jr., H. D. Eaton, C. F. Helmboldt, E. L. Jungherr, S. A. Robrish, G. Beall, and L. A. Moore Relative value of carotene from alfalfa and vitamin A from a dry carrier fed at minimum levels to Holstein calves. J. Dairy Sci. 37: Schams, D., B. Horrmanm, K. H. Lotthammer, and L. Ahlswede Untersuchungen uber eine spezifische Vitamin A-unabhangige Wirkung des/3- Carotins auf die Fertilitat des Rindes. 4. Mitt.: Auswirkung auf hormonale Parameter. Dtsch. Tieraerztl. Wochenschr. 84: Snyder, W. E., and R. L. Stuart Nutritional role of beta-carotene in bovine fertility. J. Dairy Sci. 64(Suppl. 1):104. (Abstr.) 34 Sutton, T. S., W. E. Krauss, and S. L. Hansard The effect of vitamin A deficiency on the young male bovine. J. Dairy Sci. 23 : Tomlinson, J. E., R. W. Hemken, G. E. Mitchell, Jr., and R. E. Tucker Mammary transfer of vitamin A alcohol and ester in lactating dairy cows. J. Dairy Sci. 59: Ullrey, D. E Biological availability of fatsoluble vitamins: vitamin A and carotene. J. Anim. Sci. 35: Ward, R. E., S. i. Bechdel, and N. B, Guerrant Carotene and vitamin A in the nutrition of growing dairy cattle. J. Dairy Sci. 23 : 115.