The Fate of Synthetic and Endogenous Hormones Used in the US Beef and Dairy Industries and the Potential for Human Exposure

Abstract

Purpose of Review

Growth-enhancing chemicals used by the beef and dairy industries may be bioavailable to humans via milk, meat, and other environmental matrices. This review evaluates the potential for environmental transport and bioavailability of the active chemical to humans.

Recent Findings

Bovine somatostatin is detectable in milk; however, there is no evidence that the protein persists in the environment nor that it is active in humans. In contrast, steroids are transported through milk and meat to humans where they may exert biological activity. Furthermore, environmental matrices such as raw water and dust may also allow for the environmental transport and bioavailability of steroids to humans.

Summary

Endogenous and exogenous steroids can be found in the meat, milk, and waste materials produced by cattle. While the concentrations may be low, exposure to these matrices, most notably dairy products made with whole milk, can be a source of exogenous steroids to humans.

This is a preview of subscription content, access via your institution.

Fig. 1

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.

    Haug A, Hostmark AT, Harstad OM. Bovine milk in human nutrition—a review. Lipids Health Disease. 2007;6:25.

    Article  CAS  Google Scholar 

  2. 2.

    US Department of Health and Human Services. (2017) Foods linked to illness. https://www.cdc.gov/foodsafety/foods-linked-illness.html. Last accessed, March 5, 2018.

  3. 3.

    US Department of Health and Human Services (2012) Foodborne illnesses. NIH Publication No.-12–4730. Available at: www.digestive.niddk.nih.gov. Last accessed, March 5, 2018.

  4. 4.

    Morbidity CDC, Report MW. Human tuberculosis caused by Mycobacterium bovis—New York City, 2001-2004. June 24. 2005;54(24):605–8.

    Google Scholar 

  5. 5.

    Kolok AS, Sellin MK. The environmental impact of growth-promoting compounds employed by the United States beef cattle industry: history, current knowledge, and future directions. In: Reviews of environmental contamination and toxicology, vol. 195; 2008. p. 1–30.

    Google Scholar 

  6. 6.

    Jones SJ, Johnson RD, Calkins CR, Dikeman ME. Effects of trenbolone acetate on carcass characteristics and serum testosterone in bulls and steers on different management and implant schemes. J Anim Sci. 1991;69:1363–9.

    Article  PubMed  CAS  Google Scholar 

  7. 7.

    Lone KP. 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. 1997;37:93–209.

    Article  CAS  Google Scholar 

  8. 8.

    Rumsey TS, Tyrrell HF, Dinius DA, Moe PW, Cross HR. Effect of diethylstilbestrol on tissue gain and carcass merit of feedlot beef steers. J Anim Sci. 1981;53:589–600.

    Article  PubMed  CAS  Google Scholar 

  9. 9.

    Herbst AL, Ulfelder H, Poskanzer DC. Adenocarcinomas of the vagina: association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med. 1971;284:878–81.

    Article  PubMed  CAS  Google Scholar 

  10. 10.

    Wade N. DES: a case of regulatory abdication. Science. 1972;177:335–7.

    Article  PubMed  CAS  Google Scholar 

  11. 11.

    Epstein SS. The chemical jungle: today’s beef industry. Int J Health Sci. 1990;20:277–80.

    CAS  Google Scholar 

  12. 12.

    Butler LJ. The profitablility of rBST on U.S. dairy farms. AgBioforum. 1999;2(2):111–7.

    Google Scholar 

  13. 13.

    Taur et al. The effect of bovine somatotropin on the cost of producing milk: estimates using propensity scores. J Dairy Sci. 2016;99(4):2979–85. https://doi.org/10.3168/jds.2015-9942.

    Article  CAS  Google Scholar 

  14. 14.

    U.S. Department of Agriculture. (2008) Dairy. Part III: reference of dairy cattle health and management practices in the United States, 2007 USDA–APHIS–VS, CEAH. Fort Collins. CO #N482. 2007:0908.

  15. 15.

    USDA. 2016. Dairy 2014, “Dairy Cattle Management Practices in the United States, 2014” USDA–APHIS–VS–CEAH–NAHMS. Fort Collins, CO #692.0216.

  16. 16.

    American Cancer Society. (2017) Recombinant bovine growth hormone. https://www.cancer.org/cancer/cancer-causes/recombinant-bovine-growth-hormone.html. Last accessed, December 2, 2017

  17. 17.

    Bauman DE. Bovine somatotropin: review of an emerging animal technology. J Dairy Sci. 1992;75(12):3432–51. https://doi.org/10.3168/jds.S0022-0302(92)78119-3.

    Article  PubMed  CAS  Google Scholar 

  18. 18.

    Parodi PW. Dairy product consumption and the risk of prostate cancer. Int Dairy J. 2009;19(10):551–65. https://doi.org/10.1016/j.idairyj.2009.05.006.

    Article  CAS  Google Scholar 

  19. 19.

    Sejrsen K, Pedersen LO, Vestergaard M, Purup S. Biological activity of bovine milk contribution of igf-i and igf binding proteins. Livest Prod Sci. 2001;70(1–2):79–85. https://doi.org/10.1016/S0301-6226(01)00199-3.

    Article  Google Scholar 

  20. 20.

    Meyer Z, Höflich C, Wirthgen E, Olm S, Hammon HM, Hoeflich A. Analysis of the IGF-system in milk from farm animals—occurrence, regulation, and biomarker potential. Growth Hormone and IGF Research. 2017;35:1–7. https://doi.org/10.1016/j.ghir.2017.05.004.

    Article  PubMed  CAS  Google Scholar 

  21. 21.

    Collier RJ, Bauman DE. Update on human health concerns of recombinant bovine somatotropin use in dairy cows. J Anim Sci. 2014;92(4):1800–7. https://doi.org/10.2527/jas2013-7383.

    Article  PubMed  CAS  Google Scholar 

  22. 22.

    Lampe JW. Dairy products and cancer. J Am Coll Nutr. 2011;30:464S–70S. https://doi.org/10.1080/07315724.2011.10719991.

    Article  PubMed  CAS  Google Scholar 

  23. 23.

    Larsson SC, Crippa A, Orsini N, Wolk A, Michaëlsson K. Milk consumption and mortality from all causes, cardiovascular disease, and cancer: a systematic review and meta-analysis. Nutrients. 2015;7(9):7749–63. https://doi.org/10.3390/nu7095363.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. 24.

    Thorning TK, Raben A, Tholstrup T, Soedamah-Muthu SS, Givens I, Astrup A. Milk and dairy products: good or bad for human health? An assessment of the totality of scientific evidence. Food and Nutrition Research. 2016;60:32527. https://doi.org/10.3402/fnr.v60.32527.

    Article  PubMed  CAS  Google Scholar 

  25. 25.

    Rowlands M, Gunnell D, Harris R, Vatten LJ, Holly JMP, Martin RM. Circulating insulin-like growth factor peptides and prostate cancer risk: a systematic review and meta-analysis. Int J Cancer. 2009;124(10):2416–29. https://doi.org/10.1002/ijc.24202.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. 26.

    • Harrison S, Lennon R, Holly J, Higgins JPT, Gardner M, Perks C, et al. Does milk intake promote prostate cancer initiation or progression via effects on insulin-like growth factors (IGFs)? A systematic review and meta-analysis. Cancer Causes and Control. 2017;28(6):497–528. https://doi.org/10.1007/s10552-017-0883-1. The study conducted a meta-analysis concluding that IGF-I is a potential mechanism underlying the observed associations between milk intake and prostate cancer risk.

    Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Qin L, Wang P, Kaneko T, Hoshi K, Sato A. Estrogen: one of the risk factors in milk for prostate cancer. Med Hypotheses. 2004;62(1):133–42. https://doi.org/10.1016/S0306-9877(03)00295-0.

    Article  PubMed  CAS  Google Scholar 

  28. 28.

    Hartmann S, Lacorn M, Steinhart H. Natural occurrence of steroid hormones in food. Food Chem. 1998;62:7–20.

    Article  CAS  Google Scholar 

  29. 29.

    Yu C, Deeb RA, Chu K. Microbial degradation of steroidal estrogens. Chemosphere. 2013;91(9):1225–35. https://doi.org/10.1016/j.chemosphere.2013.01.112.

    Article  PubMed  CAS  Google Scholar 

  30. 30.

    Fritsche S, Rumsey TS, Meyer HHD, Schmidt G, Steinhart H. Profiles of steroid hormones in beef from steers implanted with Synovex-S (estradiol benzoate and progesterone) in comparison to control steers. Z Lebensm Unters Forsch A. 1999;208:328–31.

    Article  CAS  Google Scholar 

  31. 31.

    Courant F, Antignac J, Laille J, Monteau F, Andre F, Le Bizec B. Exposure assessment of prepubertal children to steroid endocrine disruptors. 2. Determination of steroid hormones in milk, egg, and meat samples. J Agric Food Chem. 2008;56(9):3176–84. https://doi.org/10.1021/jf800096f.

    Article  PubMed  CAS  Google Scholar 

  32. 32.

    Adamusova H, Bosakova Z, Coufal P, Pacakova V. Analysis of estrogens and estrogen mimics in edible matrices—a review. J Sep Sci. 2014;37(8):885–905. https://doi.org/10.1002/jssc.201301234.

    Article  PubMed  CAS  Google Scholar 

  33. 33.

    Goyon A, Cai JZ, Kraehenbuehl K, Hartmann C, Shao B, Mottier P. Determination of steroid hormones in bovine milk by LC-MS/MS and their levels in Swiss Holstein cow milk. Food Additives and Contaminants - Part A Chemistry, Analysis, Control, Exposure and Risk Assessment. 2016;33(5):804–16.

    CAS  Google Scholar 

  34. 34.

    Xu L, Zhang L, Zhang Y, Sheng Q, Zhao A. Qualitative and quantitative comparison of hormone contents between bovine and human colostrums. Int Dairy J. 2011;21(1):54–7. https://doi.org/10.1016/j.idairyj.2010.04.006.

    Article  CAS  Google Scholar 

  35. 35.

    Macrina AL, Ott TL, Roberts RF, Kensinger RS. Estrone and estrone sulfate concentrations in milk and milk fractions. J Acad Nutr Diet. 2012;112(7):1088–93. https://doi.org/10.1016/j.jand.2012.02.005.

    Article  PubMed  CAS  Google Scholar 

  36. 36.

    Yang Y, Shao B, Zhang J, Wu Y, Duan H. Determination of the residues of 50 anabolic hormones in muscle, milk and liver by very-high-pressure liquid chromatography-electrospray ionization tandem mass spectrometry. J Chromatogr B Anal Technol Biomed Life Sci. 2009;877(5–6):489–96. https://doi.org/10.1016/j.jchromb.2008.12.054.

    Article  CAS  Google Scholar 

  37. 37.

    Vandenberg, L. N., Colborn, T., Hayes, T. B., Heindel, J. J., Jacobs, D. R., Lee, D. -., . . . Myers, J. P. (2012) Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev, 33(3), 378–455. doi:https://doi.org/10.1210/er.2011-1050.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. 38.

    U.S. Department of Health and Human Services and U.S. Department of Agriculture. 2015 – 2020 dietary guidelines for Americans. In: 8th edition; 2015. https://health.gov/dietaryguidelines/2015/guidelines/.

    Google Scholar 

  39. 39.

    Archer, D. F., Nakajima, S. T., Sawyer, A. T., Wentworth, J., Trupin, S., Koltun, W. D., . . . Ellman, H. (2013) Norethindrone acetate 1.0 milligram and ethinyl estradiol 10 micrograms as an ultra low-dose oral contraceptive. Obstet Gynecol, 122(3), 601–607. doi:https://doi.org/10.1097/AOG.0b013e3182a1741c.

    Article  PubMed  CAS  Google Scholar 

  40. 40.

    Hammond GL. Plasma steroid-binding proteins: primary gatekeepers of steroid hormone action. J Endocrinol. 2016;230(1):R13–25. https://doi.org/10.1530/JOE-16-0070.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. 41.

    U.S. Food and Drug Administration. (2017) Steroid hormone implants used for growth in food-producing animals. October 2017. https://www.fda.gov/AnimalVeterinary/SafetyHealth/ProductSafetyInformation/ucm055436.htm Last Accessed: December 1, 2017.

  42. 42.

    IARC, (1987) Overall evaluations of carcinogenicity: an updating of IARC Monographs Volumes 1 to 42. Supplement No 7. International Agency for Research on Cancer, Lyon.

  43. 43.

    IARC, (1995) Monographs on the Evaluation of the carcinogenic risks to humans. Sex Hormones 21, International Agency for Research on Cancer, Lyon.

  44. 44.

    Lipschutz A, Vargas L Jr. Structure and origin of uterine and extragenital fibroids induced experimentally in the guinea pig by prolonged administration of estrogens. Cancer Res. 1994;1:236–48.

    Google Scholar 

  45. 45.

    Perez-Comas A. Premature sexual development in Puerto Rico. Boletin Asociacion Medicade Puerto Rico. 1988;80:85–90.

    CAS  Google Scholar 

  46. 46.

    Saenz de Rodriguez CA, Bongiovanni AM, Conde de Borrego L. An epidemic of precocious development in Puerto Rican children. J Pediatr. 1985;107:393–6.

    Article  PubMed  CAS  Google Scholar 

  47. 47.

    Fara, G.M., De. Corvo, G., Bernuzzi, S., Bigatello, A., Di Pietro, C., Scaglioni, S., Chiumello, G. Epidemic of breast enlargement in an Italian school. Lancet. August. 1979;11:295–7.

    Google Scholar 

  48. 48.

    Pasquino AM, Balducci R, Manca Bitti ML, Spadoni GL, Boscherini B. Transient pseudo-precocious puberty by probably oestrogen intake in 3 girls. Arch Dis Child. 1982;57:954–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. 49.

    Abete I, Romaguera D, Vieira AR, Lopez de Munain A, Norat T. Association between total, processed, red and white meat consumption and all cause, CVD and IHD mortality: a meta-analysis of cohort studies. Britian Journal of Nutrition. 2014;112:762–75.

    Article  CAS  Google Scholar 

  50. 50.

    • Lippi, G., C. Mattiuzzi, G. Cervellin. (2016) Meat consumption and cancer risk: a critical review of published meta-analyses critical reviews in oncology/hematology 97: 1–14. This study conducted a meta-analysis that found an association between beef consumption and cancer.

    Google Scholar 

  51. 51.

    US Census of Agriculture. 2012. Available at: https://www.agcensus.usda.gov/Publications/2012/ Last accessed, March 5, 2018.

  52. 52.

    Barker, J.C. and F.R. Walls. 2002. Livestock manure productin rates and nutrient content. 2002 North Carolina Agricultural Chemicals Manual. Available at: (http://agrienvarchive.ca/bioenergy/download/barker_ncsu_manure_02.pdf). Last accessed, March 5, 2018.

  53. 53.

    Bartelt-Hunt SL, Snow DD, Kranz WL, Mader TL, Shapiro CA, van Donk SJ, et al. Effect of growth promotants on the occurrence of natural and synthetic steroid hormones on feedlot soils and in runoff from beef cattle feeding operations. Environ Sci Technol. 2012;46(3):1352–60.

    Article  PubMed  CAS  Google Scholar 

  54. 54.

    Schiffer B, Daxenberger A, Meyer K, Meyer HHD. The fate of Trenbolone acetate and Melengesterol acetate as growth promoters in cattle: environmental studies. Environ Health Perspect. 2001;109:1145–51.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. 55.

    Noguera-Oviedo KM, Aga DS. Chemical and biological assessment of endocrine disrupting chemicals in a full scale dairy manure anaerobic digester with thermal pretreatment. Sci Total Environ. 2016;550:827–34.

    Article  PubMed  CAS  Google Scholar 

  56. 56.

    Zheng W, Yates SR, Bradford SA. Analysis of steroid hormones in a typical dairy waste disposal system. Environ Sci Technol. 2008;42:530–5.

    Article  PubMed  CAS  Google Scholar 

  57. 57.

    Havens SM, Hedman CJ, Hemming JDC, Miertz MG, Shafer MM, Schauer JJ. Stability, preservation and quantification of hormones and estrogenic and androgenic activities in surface water runoff. Environ Toxicol Chem. 2010;29:2481–90.

    Article  PubMed  CAS  Google Scholar 

  58. 58.

    Kolodziej EP, Harter T, Sedlak DL. Dairy wastewater, aquaculture and spawning fish as sources of steroid hormones in the aquatic environment. Environ Sci Technol. 2004;38:6377–84.

    Article  PubMed  CAS  Google Scholar 

  59. 59.

    Lorenzen A, Hendel JG, Conn KL, Bittman S, Swabiah AB, Lazarovitz G, et al. Survey of hormone activities in municipal biosolids and animal manures. Environ Toxicol. 2004;19:216–25.

    Article  PubMed  CAS  Google Scholar 

  60. 60.

    Sangster JL, Ali JM, Snow DD, Kolok AS, Bartelt-Hunt SL. Bioavailability and fate of sediment-associated progesterone in aquatic systems. Environ Sci Technol. 2016;50(7):4027–36.

    Article  PubMed  CAS  Google Scholar 

  61. 61.

    CDC. 2014. Drinking water. Private ground water wells. https://www.cdc.gov/healthywater/drinking/private/wells/index.html). Last Accessed, March 5, 2018.

  62. 62.

    Arnon S, Dahan O, Elhanany S, Cohen K, Pankratov I, Gross A, et al. Transport of testosterone and estrogen from dairy-farm waste lagoons to groundwater. Environ Sci Technol. 2008;42:5521–6.

    Article  PubMed  CAS  Google Scholar 

  63. 63.

    Kolodziej EP, Sedlak DL. Rangeland grazing as a source of steroid hormones to surface waters. Environ Sci Technol. 2007;41:3514–20.

    Article  PubMed  CAS  Google Scholar 

  64. 64.

    Bartelt-Hunt SL, Snow DD, Damon-Powell TR, Meisbach D. Occurrence of steroid hormones and antibiotics in shallow groundwater impacted by livestock waste control facilities. J Contam Hydrol. 2011;123:94–103.

    Article  PubMed  CAS  Google Scholar 

  65. 65.

    •• Blackwell, B.R., K.J. Wooten, M.D. Buser, B.J. Johnson, G.P. Cobb, and P.N. Smith. (2015) Occurrence and characterization of steroid growth promoters associated with particulate matter originating from beef cattle feedyards. Environmental science and technology. Environ. Sci. Technol., 2015, 49 (14), pp 8796–8803. This study provides evidence that dusts blown from feedlot operations contain steroidal growth promoting compounds.

    Google Scholar 

  66. 66.

    Wooten KJ, Blackwell BR, McEachran AD, Mayer GD, Smith PN. Airborne particulate matter collected near beef cattle feedyards induces androgenic and estrogenic activity in vitro. Agric Ecosyst Environ. 2015;203:29–35. https://doi.org/10.1016/j.agee.2015.01.016.

    Article  CAS  Google Scholar 

  67. 67.

    Kirkhorn SR, Garry VF. Agricultural lung diseases. Environ Health Perspect. 2000;108(Suppl. 4):705–12.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Alan S. Kolok.

Ethics declarations

Conflict of Interest

Alan S. Kolok, Jonathan M. Ali, Eleanor G. Rogan, and Shannon L. Bartelt-Hunt declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

This article is part of the Topical Collection on Food, Health, and the Environment

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kolok, A.S., Ali, J.M., Rogan, E.G. et al. The Fate of Synthetic and Endogenous Hormones Used in the US Beef and Dairy Industries and the Potential for Human Exposure. Curr Envir Health Rpt 5, 225–232 (2018). https://doi.org/10.1007/s40572-018-0197-9

Download citation

Keywords

  • Beef
  • Dairy
  • Exogenous hormones
  • Bioavailability