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The Environmental Impact of Growth-Promoting Compounds Employed by the United States Beef Cattle Industry: History, Current Knowledge, and Future Directions

  • Alan S. Kolok
  • Marlo K. Sellin
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 195)

Recent publications in the popular literature (Renner 2002; Raloff 2002) have suggested that the growth-promoting compounds used on beef cattle in the United States may have significant impacts on local aquatic environments. Clearly, beef cattle held in finishing feedlots represent a greater environmental risk than do pasture-fed cattle for at least two principal reasons. First, cattle in feedlots are held at much higher concentrations than on pastureland. Second, most cattle in feedlots are administered high-potency growth-promoting compounds (Montgomery et al. 2001). Research has shown that these compounds can travel in the environment (Lange et al. 2002) and that they may cause endocrine-disrupting effects on local fish populations (Orlando et al. 2004).

In this review, our principal hypothesis is that the environmental risks associated with finishing beef cattle feedlots are best dealt with when there is a thorough understanding of (1) the implant strategies used at feedlots, (2) the environmental fate of the growth-promoting compounds used on the feedlot, and (3) the effect that these growth promoters have on fishes should they reach surface waters. This chapter reviews the current state of knowledge and points out areas where additional research is warranted.

Keywords

Beef Cattle Poultry Litter Fathead Minnow Japanese Medaka Polar Organic Integrative Chemical Sampler 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Al-Ablani SA, Phelps RP (2002) Paradoxes in exogenous androgen treatments of bluegill. J Appl Ichthyol 18:61–64.CrossRefGoogle Scholar
  2. Ankley GT, Jensen KM, Makynen EA, Kahl MD, Korte JJ, Hornung MW, Henry TR, Denny JS, Leino RL, Wilson VS, Cardon MC, Hartig PC, Gray LE (2003) Effects of the androgenic growth promoter 17-β-trenbolone on fecundity and reproductive endocrinology of the fathead minnow. Environ Toxicol Chem 22:1350–1360.CrossRefGoogle Scholar
  3. Ankley GT, Defoe DL, Kahl MD, Jensen KM, Makynen EA, Miracle A, Hartig P, Gray LE Cardon M, Wilson V (2004) Evaluation of the model anti-androgen flutamide for assessing the mechanistic basis of responses to an androgen in the fathead minnow (Pimephales promelas). Environ Sci Technol 38:6322–6327.CrossRefGoogle Scholar
  4. Arslan T, Phelps RP (2004a) Directing gonadal differentiation in bluegill, Lepomis macrochirus (Rafinesque), and black crappie, Pomoxis nigromaculatus (Lesueur), by periodic estradiol-171 immersions. Aquac Res 35:397–402.CrossRefGoogle Scholar
  5. Arslan T, Phelps RP (2004b) Production of monosex male black crappie, Pomoxis nigromaculatus, populations by multiple androgen immersion. Aquaculture 234:561–573.CrossRefGoogle Scholar
  6. Arukwe A, Kullman SW, Hinton DE (2001) Differential biomarker gene and protein expressions in nonylphenol and estradiol-17β treated juvenile rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol 129C:1–10.Google Scholar
  7. Balch GC, Shami K, Wilson PJ, Wakamatsu Y, Metcalfe CD (2004) Feminization of female leukophore-free strain of Japanese medaka (Oryzias latipes) exposed to 17β-estradiol. Environ Toxicol Chem 23:2763–2768.CrossRefGoogle Scholar
  8. Belfroid AC, Van der Horst A, Vathaak AD, Schafer AJ, Rijs GBJ, Wegener J, Cofino WP (1999) Analysis and occurrence of estrogenic hormones and their glucuronides in surface water and waste water in The Netherlands. Sci Total Environ 225:101–108.CrossRefGoogle Scholar
  9. Brion F, Tyler CR, Palazzi X, Laillet B, Porcher JM, Garric J, Flammarion P (2004) Impacts of 17β-estradiol, including environmentally relevant concentrations, on reproduction after exposure during embryo-larval-, juvenile- and adult-life stages in zebrafish (Danio rerio). Aquat Toxicol 68:193–217.CrossRefGoogle Scholar
  10. Casey FXM, Larsen GL, Hakk H, Simunek J (2003) Fate and transport of 17β-estradiol in soil-water systems. Environ Sci Technol 37:2400–2409.CrossRefGoogle Scholar
  11. Casey FXM, Hakk H, Simunek J, Larsen GL (2004) Fate and transport of testosterone in agricultural soils. Environ Sci Technol 38:790–798.CrossRefGoogle Scholar
  12. Colucci MS, Topp E (2002) Dissipation of part-per-trillion concentrations of estrogenic hormones from agricultural soils. Can J Soil Sci 82:335–340.Google Scholar
  13. Colucci MS, Bork H, Topp E (2001) Persistence of estrogenic hormones in agricultural soils: I. 17β-Estradiol and estrone. J Environ Qual 30:2070–2076.Google Scholar
  14. Das BS, Lee LS, Rao PSC, Hultgren RP (2004) Sorption and degradation of steroid hormones in soils during transport: column studies and model evaluation. Environ Sci Technol 38:1460–1470.CrossRefGoogle Scholar
  15. D’Ascenzo G, Di Corcia A, Gentili A, Mancini R, Mastropasqua R, Nazzari M, Samperi R (2003) Fate of natural estrogen conjugates in municipal sewage transport and treatment facilities. Sci Total Environ 302:199–209.CrossRefGoogle Scholar
  16. Durhan EJ, Lambright CS, Makynen EA, Lazorchak J, Hartig PC, Wilson VS, Gray LE, Ankley GT (2006) Identification of metabolites of trenbolone acetate in androgenic runoff from a beef feedlot. Environ Health Perspect 114(suppl 1):65–68.Google Scholar
  17. Epstein SS (1990) The chemical jungle: today’s beef industry. Int J Health Sci 20:277–280.Google Scholar
  18. Estergreen VL, Lin MT, Martin EL, Moss GE, Branen AL, Luedecke LO, Shimoda W (1977) Distribution of progesterone and its metabolites in cattle tissues following administration of progesterone-4–C1, 2, 3, 4. J Anim Sci 46:642–651.Google Scholar
  19. Filby AL, Tyler CR (2005) Molecular characterization of estrogen receptors 1, 2a, and 2b and their tissue and ontogenic expression profiles in fathead minnow (Pimephales promelas). Biol Reprod 73:648–662.CrossRefGoogle Scholar
  20. Finlay-Moore O, Hartel PG, Cabrera ML (2000) 17β-Estradiol and testosterone in soil and runoff from grasslands amended with broiler litter. J Environ Qual 29:1604–1611.CrossRefGoogle Scholar
  21. Foutz CP, Dolezal HG, Gardner TL, Gill DR, Hensley JL, Morgan JB (1997) Anabolic implant effects on steer performance, carcass traits, subprimal yields, and longissimus muscle properties. J Anim Sci 75:1256–1265.Google Scholar
  22. Galvez JI, Mazik PM, Phelps RP, Mulvaney DR (1995) Masculinization of channel catfish Ictalurus punctatus by oral administration of trenbolone acetate. J World Aquat Sci 26:378–383.CrossRefGoogle Scholar
  23. Galvez JI, Morrison JR, Phelps RP (1996) Efficacy of trenbolone acetate in sex inversion of the blue tilapia Oreochromis aureus. J World Aquac Soc 27:483–486.CrossRefGoogle Scholar
  24. Hahlbeck E, Katsiadaki I, Mayer I, Adolfsson-Erici M, James J, Bengtsson BE (2004) The juvenile three-spined stickleback (Gasterosteus aculeatus L.) as a model organism for endocrine disruption II: kidney hypertrophy, vitellogenin and spiggin induction. Aquat Toxicol 70:311–326.CrossRefGoogle Scholar
  25. Hartley WR, Thiyagarajah A, Anderson MB, Broxson MW, Major SE, Zell SI (1998) Gonadal development in Japanese medaka (Oryzias latipes) exposed to 17β-estradiol. Mar Environ Res 46:145–148.CrossRefGoogle Scholar
  26. Herbst AL, Ulfelder H, Poskanzer DC (1971) Adenocarcinomas of the vagina: association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med 284:878–881.Google Scholar
  27. Hermesmeyer GN, Berger LL, Nash TG, Brandt Jr. RT (2000) Effects of energy intake, implantation, and subcutaneous fat end point on feedlot steer performance and carcass composition. J Anim Sci 78:825–831.Google Scholar
  28. Hirai N, Nanba A, Koshio M, Kondo T, Mortia M, Tatarazako N (2006) Feminization of Japanese medaka (Oryzias latipes) exposed to 17-beta-estradiol: formation of testis-ova and sex-transformation during early-ontogeny. Aquat Toxicol 77:78–86.CrossRefGoogle Scholar
  29. Holbech H, Kinnberg K, Petersen GI, Jackson P, Hylland K, Norrgren L, Bjerregaard P (2006) Detection of endocrine disrupters: evaluation of a fish sexual development test (FSDT). Comp Biochem Physiol 144C:57–66.Google Scholar
  30. Hook SE, Skillman AD, Small JE, Schultz IR (2006) Gene expression patterns in rainbow trout, Oncorhyncus mykiss, exposed to a suite of model toxicants. Aquat Toxicol 77:372–385.CrossRefGoogle Scholar
  31. Imai S, Koyama J, Fujii K (2005) Effects of 17β-estradiol on the reproduction of Java-medaka (Oryzias javanicus), a new test fish species. Mar Pollut Bull 51:708–714.CrossRefGoogle Scholar
  32. Imai S, Koyama J, Fujii K (2007) Effects of estrone on full life cycle of java medaka (Oryzias javanicus), a new marine test fish. Environ Toxicol Chem 26:726–731.CrossRefGoogle Scholar
  33. Irwin LK, Gray S, Oberdorster E (2001) Vitellogenin induction in painted turtle, Chrysemys picta, as a biomarker of exposure to environmental levels of estradiol. Aquat Toxicol 55:49–60.CrossRefGoogle Scholar
  34. Ivie GW, Christopher RJ, Munger CE, Coppock CE (1986) Fate and residues of [4-14C]estradiol-17C after intrasmuscular injection into Holstein steer calves. J Anim Sci 62:681–690.Google Scholar
  35. Jacobsen A-M, Lorenzen A, Chapman R, Topp E (2005) Persistence of testosterone and 17β-estradiol in soils receiving swine manure or municipal biosolids. J Environ Qual 34:861–871.CrossRefGoogle Scholar
  36. Jensen KM, Makynen EA, Kahl MD, Ankley GT (2006) Effects of the feedlot contaminant 17α-trenbolone on reproductive endocrinology of the fathead minnow. Environ Sci Technol 40:3112–3117.CrossRefGoogle Scholar
  37. Jones SJ, Johnson RD, Calkins CR, Dikeman ME (1991) Effects of trenbolone acetate on carcass characteristics and serum testosterone in bulls and steers on different management and implant schemes. J Anim Sci 69:1363–1369.Google Scholar
  38. Kim I, Yu Z, Xiao B, Huang W (2007) Sorption of male hormones by soils and sediments. Environ Toxicol Chem 26:264–270.CrossRefGoogle Scholar
  39. Kolodziej EP, Harter T, Sedlak DL (2004) Dairy wastewater, aquaculture, and spawning fish as sources of steroid hormones in the aquatic environment. Environ Sci Technol 38:6377–6384.CrossRefGoogle Scholar
  40. Kolok AS, Snow DD, Kohno S, Sellin MK, Guillette LJ Jr (2007) Occurrence and biological effect of exogenous steroids in the Elkhorn River, Nebraska. Sci Total Environ 388:104–115.CrossRefGoogle Scholar
  41. Kramer VJ, Miles-Richardson S, Pierens SL, Giesy JP (1998) Reproductive impairment and induction of alkaline-labile phosphate, a biomarker of estrogen exposure, in fathead minnows (Pimephales promelas) exposed to waterborne 17β-estradiol. Aquat Toxicol 40:335–360.CrossRefGoogle Scholar
  42. Krzeminski LF, Cox BL, Gosline RE (1981) Fate of radioactive melengestrol acetate in the bovine. J Agric Food Chem 29:387–391.CrossRefGoogle Scholar
  43. Lange IG, Daxenbarger A, Schiffer B, Witters H, Ibarreta D, Meyer HHD (2002) Sex hormones originating from different livestock production systems: fate and potential disrupting activity in the environment. Anal Chem Acta 473:27–37.CrossRefGoogle Scholar
  44. Larkin P, Sabo-Attwood T, Kelso J, Denslow ND (2002) Gene expression analysis of largemouth bass exposed to estradiol, nonylphenol, and p,p’-DDE. Comp Biochem Physiol 133B:543–557.Google Scholar
  45. Lee CY, Henricks DM, Skelley GC, Grimes LW (1990) Growth and hormonal response of intact and castrate male cattle to trenbolone acetate and estradiol. J Anim Sci 68:2682–2689.Google Scholar
  46. Lee LS, Strock TJ, Sarmah AK, Rao PSC (2003) Sorption and dissipation of testosterone, estrogens, and their primary transformation products in soils and sediments. Environ Sci Technol 37:4098–4105.CrossRefGoogle Scholar
  47. LeGuevel R, Pakdel F (2001) Assessment of oestrogenic potency of chemicals used as growth promoter by in-vitro methods. Human Reprod 16:1030–1036.CrossRefGoogle Scholar
  48. Loomis AK, Thomas P (2000) Effects of estrogens and xenoestrogens on androgen production by Atlantic croaker testes in vitro: evidence for a nongenomic action mediated by an estrogen membrane receptor. Biol Reprod 62:995–1004.CrossRefGoogle Scholar
  49. Lone KP (1997) Natural sex steroids and the xenobiotic analogs in animal production: growth, carcass quality, pharmacokinetics, metabolism, mode of action, residues, methods and epidemiology. Crit Rev Food Sci 37:93–209.CrossRefGoogle Scholar
  50. Lorenzen A, Hendel JG, Conn KL, Bittman S, Kwabiah AB, Lazarovitz G, Masse D, McAllister TA, Topp E (2004) Survey of hormone activities in municipal biosolids and animal manures. Environ Toxicol 19:216–225.CrossRefGoogle Scholar
  51. Lorenzen A, Chapman R, Hendel JG, Topp E (2005) Persistence and pathways of testosterone dissipation in agricultural soil. J Environ Qual 34:854–860.CrossRefGoogle Scholar
  52. Matthiessen P, Arnold D, Johnson AC, Pepper TJ, Pottinger TG, Pulman KGT (2006) Contamination of headwater streams in the United Kingdom by oestrogenic hormones from livestock farms. Sci Total Environ 367:616–630.CrossRefGoogle Scholar
  53. Mellin TN, Erb RE (1966a) Estrogen metabolism and excretion during the bovine estrous cycle. Steroids 7:589–603.CrossRefGoogle Scholar
  54. Mellin TN, Erb RE (1966b) Estrogens in the bovine: a review. J Dairy Sci 48:687–700.CrossRefGoogle Scholar
  55. Meyer HHD (2001) Biochemistry and physiology of anabolic hormones used for improvement of meat production. APMIS 8:1–8.CrossRefGoogle Scholar
  56. Miles-Richardson SR, Kramer VJ, Fitzgerald SD, Render JA, Yamini B, Barbee SJ, Giesy JP (1999) Effects of waterborne exposure of 17β-estradiol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Aquat Toxicol 47:129–145.CrossRefGoogle Scholar
  57. Miller DH, Jensen KM, Villeneuve DL, Kahl MD, Makynen EA, Durhan EJ, Ankley GT (2007) Linkage of biochemical responses to population-level effects: a case study with vitellogenin in the fathead minnow (Pimephales promelas). Environ Toxicol Chem 26:521–527.CrossRefGoogle Scholar
  58. Mills LJ, Gutjahr-Gobell RE, Horowitz DB, Denslow ND, Chow MC, Zaroogian GE (2003) Relationship between reproductive success and male plasma vitellogenin concentrations in cunner, Tautogolabrus adspersus. Environ Health Perspect 111:93–99.Google Scholar
  59. Miracle A, Ankley G, Lattier D (2006) Expression of two vitellogenin genes (vg1 and vg3) in fathead minnow (Pimephales promelas) liver in response to exposure to steroidal estrogens and androgens. Ecotoxicol Environ Saf 63:337–342.CrossRefGoogle Scholar
  60. Miura T, Higuchi M, Ozaki Y, Ohta T, Miura C (2006) Progestin is an essential factor for the initiation of the meiosis in spermatogenetic cells of the eel. Proc Natl Acad Sci U S A 103:7333–7338.CrossRefGoogle Scholar
  61. Moens LN, van der Ven K, Van Remortel P, Del-Favero J, De Coen WM (2006) Expression profiling of endocrine-disrupting compounds using a customized Cyprinus carpio cDNA microarray. Toxicol Sci 93:298–310.CrossRefGoogle Scholar
  62. Montgomery TH, Dew PF, Brown MS (2001) Optimizing carcass value and the use of anabolic implants in beef cattle. J Anim Sci 79(suppl E):E296–E306.Google Scholar
  63. Nayak PK, Mishra J, Ayyappan S, Singh BN (2001) 17α-Hydroxyl progesterone-induced breeding of the stinging catfish Heteropneustes folssilis (Bolch) with or without priming of gonadotropin. J Aquat Trop 16:159–164.Google Scholar
  64. Nichols DJ, Daniel TC, Moore Jr. PA, Edwards DR, Pote DH (1997) Runoff of estrogen hormone 17β-estradiol from poultry litter applied to pasture. J Environ Qual 26:1002–1006.CrossRefGoogle Scholar
  65. Orlando EF, Kolok AS, Binzcik G, Gates J, Horton MK, Lambright C, Gray LE, Guillette LJ (2004) Endocrine disrupting effects of cattle feedlot effluent on an aquatic sentinel species, the fathead minnow. Environ Health Perspect 112:353–358.CrossRefGoogle Scholar
  66. Orn S, Yamani S, Norrgren L (2006) Comparison of vitellogenin induction, sex ratio, and gonad morphology between zebrafish and Japanese medaka after exposure to 17α-ethinylestradiol and 17β-trenbolone. Arch Environ Contam Toxicol 51:237–243.CrossRefGoogle Scholar
  67. Panter GH, Thompson RS, Sumpter JP (1998) Adverse reproductive effects in male fathead minnows (Pimephales promelas) exposed to environmentally relevant concentrations of the natural oestrogens, oestradiol and oestrone. Aquat Toxicol 42:243–253.CrossRefGoogle Scholar
  68. Parliamentary Office of Science and Technology, House of Commons, London, UK (1999) Hormones in beef. http://www.parliament.uk/post/pn127.pdf.
  69. Pelissero C, Flouriot G, Foucher JL, Bennetau B, Dunogues J, LeGac F, Sumpter JP (1993) Vitellogenin synthesis in cultured hepatocytes; an in vitro test for the estrogenic potency of chemicals. J Steroid Biochem Mol Biol 44:263–272.CrossRefGoogle Scholar
  70. Peterson EW, Davis RK, Orndorff HA (2000) 17β-Estradiol as an indicator of animal waste contamination in mantled karst aquifers. J Environ Qual 29:826–834.CrossRefGoogle Scholar
  71. Pottier J, Cousty C, Heitzman RJ, Reynolds P (1981) Differences in the biotransformation of a 17b-hydroxylated steroid, trenbolone acetate in rat and cow. Xenobiotica 11:489–500.CrossRefGoogle Scholar
  72. Preston RL (1997) Rationale for the safety of implants. http://www.fortdodgelivestock. com/pdfs/Pdfs%20for%20beef/RationaleforSafety(241).pdf.
  73. Purdy RH, Durocher CK, Moore Jr. PH, Rao PN (1980) Analysis of metabolites of progesterone in bovine liver, kidney, kidney fat, and milk by high performance liquid chromatography. J Steroid Biochem 12:1307–1315.CrossRefGoogle Scholar
  74. Raloff J (2002) Hormones: here’s the beef. Science News 161:10–12.CrossRefGoogle Scholar
  75. Renner R (2002) Do cattle growth hormones pose an environmental risk? Environ Sci Technol 36:194A–197A.CrossRefGoogle Scholar
  76. Rico AG (1983) Metabolism of endogenous and exogenous anabolic agents in cattle. J Anim Sci 57:226–232.Google Scholar
  77. Rumsey TS, Tyrrell HF, Dinius DA, Moe PW, Cross HR (1981) Effect of diethylstilbestrol on tissue gain and carcass merit of feedlot beef steers. J Anim Sci 53:589–600.Google Scholar
  78. Schiffer B, Daxenberger A, Meyer K, Meyer HHD (2001) The fate of trenbolone acetate and melengestrol acetate after application as growth promoters in cattle: environmental Studies. Environ Health Perspect 109:1145–1151.CrossRefGoogle Scholar
  79. Schwarzenberger F, Mosel E, Pamel R, Bamberg E (1996) Faecal steroid analysis for non-invasive monitoring of reproductive status in farm, wild and zoo animals. Anim Reprod Sci 42:515–526.CrossRefGoogle Scholar
  80. Seki M, Fujishima S, Nozaka T, Maeda M, Kobayashi K (2006) Comparison of response to 17β-trenbolone among three small fish species. Environ Toxicol Chem 25:2742–2752.CrossRefGoogle Scholar
  81. Shioda T, Wakabayashi M (2000) Effect of certain chemicals on the reproduction of medaka (Oryzias latipes). Chemosphere 40:239–243.CrossRefGoogle Scholar
  82. Shore LS, Gurevitz M, Shemesh M (1993) Estrogen as an environmental pollutant. Bull Environ Contam Toxicol 51:361–366.CrossRefGoogle Scholar
  83. Siemens MG (1996) Tools for optimizing feedlot production. Publication A366. Cooperative Extension, University of Wisconsin, Madison, WI.Google Scholar
  84. Sone Z, Hinage M, Itamoto M, Katsu Y, Watanabe H, Urushitani H, Tooi O, Guillette LJ Jr, Iguchi T (2005) Effects of an androgenic growth promoter 17β-trenbolone on masculinization of mosquitofish (Gambusia affinis affinis). Gen Comp Endocrinol 143:151–160.CrossRefGoogle Scholar
  85. Soto AM, Calabro JM, Prechtl NV, Yau AY, Orlando EF, Daxenberger A, Kolok AS, Guillette LJ Jr, le Bizec B, Lange IG, Sonnenschein C (2004) Androgenic and estrogenic activity in cattle feeldot effluent receiving water bodies of eastern Nebraska, USA. Environ Health Perspect 112:346–352.CrossRefGoogle Scholar
  86. Sundararaj BI, Panchanan N (1981) Steroid-induced synthesis of vitellogenin in the catfish, Heteropneustes folssilis (Bolch). Gen Comp Endocrinol 43:201–210.CrossRefGoogle Scholar
  87. Thorpe KL, Cummings RI, Hutchinson TH, Scholze M, Brighty G, Sumpter JP, Tyler CR (2003) Relative potencies and combination effects of steroidal estrogens in fish. Environ Sci Technol 37:1142–1149.CrossRefGoogle Scholar
  88. Wade N (1972) DES: A case of regulatory abdication. Science 177:335–337.CrossRefGoogle Scholar
  89. ZoBell D, Chapman CK, Heaton K, Birkelo C (2000) Beef cattle implants. Utah State University Extension Electronic Publication AG-509. <http://extension.usu.edu/htm/ publications/publication=5931>.

Copyright information

© Springer 2008

Authors and Affiliations

  • Alan S. Kolok
    • 1
  • Marlo K. Sellin
    • 2
  1. 1.Department of BiologyUniversity of Nebraska at OmahaOmahaUSA
  2. 2.Center for Environmental Toxicology986805 Nebraska Medical CenterOmahaUSA

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