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Semen Uranium Concentrations in Depleted Uranium Exposed Gulf War Veterans: Correlations with Other Body Fluid Matrices

  • Melissa A. McDiarmid
  • Patricia Gucer
  • Jose A. Centeno
  • Todor Todorov
  • Katherine S. Squibb
Article

Abstract

Environmental metal exposure, as well as dietary metals, may adversely affect semen quality even as others play an essential role in normal spermatogenesis and fertility. Measures of seminal fluid metals have therefore been of high interest in the last several decades but have shown inconsistent results in correlations with some semen quality parameters. As well, environmental metal measures across various body fluid matrices have not been consistently correlated contrary to what one might hypothesize based on a systemic body burden of metal. This may be due to the body fluid matrices assessed and to other differences in laboratory methods and sample preparation. Measures of uranium, a potentially toxic metal in humans, have not previously been reported in the semen of environmentally metal-exposed populations. We report here uranium seminal fluid results and the high correlation of uranium concentrations across several body fluid matrices in a cohort of military veterans exposed to depleted uranium in combat events during the Iraqi Gulf War. These results inform the risk communication conversation for exposed populations and broaden the public health assessments from various exposure scenarios.

Keywords

Metals Uranium Semen Biomonitoring 

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Office of the Special Assistant for Gulf War Illnesses (OSAGWI) (2000) Environmental Exposure Report: Depleted uranium in the Gulf (II). http://www.gulflink.osd.mil/du_ii/. Accessed 19 Dec 2016
  2. 2.
    Squibb KS, McDiarmid MA (2006) Depleted uranium exposure and health effects in gulf war veterans. Philos Trans R Soc Lond Ser B Biol Sci 361:639–648CrossRefGoogle Scholar
  3. 3.
    Army Environmental Policy Institute (AEPI) (1995) Health and environmental consequences of depleted uranium use in the US army. AEPI, ArlingtonGoogle Scholar
  4. 4.
    The Royal Society (2001) The health hazards of depleted uranium munitions part I Policy document 6/01Google Scholar
  5. 5.
    The Royal Society (2002) The health effects of depleted uranium munitions summary Policy document 6/02Google Scholar
  6. 6.
    National Research Council (NRC) (2008) Review of toxicologic and radiologic risks to military personnel from exposure to depleted uranium during and after combat. National Academy Press, Washington DCGoogle Scholar
  7. 7.
    Pellmar TC, Keyser DO, Emery C, Hogan JB (1999) Electrophysiological changes in hippocampal slices isolated from rats embedded with depleted uranium fragments. Neurotoxicology 20:785–892PubMedGoogle Scholar
  8. 8.
    Pellmar TC, Fuciarelli AF, Ejnik JW, Hamilton M, Hogan J, Strocko S, Emond C, Mottaz HM, Landauer MR (1999) Distribution of uranium in rats implanted with depleted uranium pellets. Toxicol Sci 49:29–39CrossRefGoogle Scholar
  9. 9.
    Arfsten DP, Still KR, Richie GD (2001) A review of the effects of uranium and depleted uranium exposure on reproduction and fetal development. Toxicol Ind Health 17:180–191.  https://doi.org/10.1191/0748233701th111oa CrossRefPubMedGoogle Scholar
  10. 10.
    Domingo JL (2001) Reproductive and developmental toxicity of natural and depleted uranium: a review. Reprod Toxicol 15:603–609CrossRefGoogle Scholar
  11. 11.
    Arfsten DP, Schaeffer DJ, Johnson EW, Cunningham JR (2006) Evaluation of the effect of implanted depleted uranium on male reproductive success, sperm concentration, and sperm velocity. Environ Rev 100:205–215 http://www.sciencedirect.com/science/article/pii/S0013935105000502?via%3Dihub Google Scholar
  12. 12.
    Araneta MR, Moore CA, Olney RS, Edmonds LD, Karcher JA, McDonough C, Hiliopoulos KM, Schlangen KM, Gray GC (1997) Goldenhar syndrome among infants born in military hospitals to gulf war veterans. Teratology 56:244–251CrossRefGoogle Scholar
  13. 13.
    Cowan DN, DeFraites RF, Gray GC, Goldenbaum MB, Wishik SM (1997) The risk of birth defects among children of Persian gulf war veterans. N Engl J Med 336:1650–1656CrossRefGoogle Scholar
  14. 14.
    Doyle P, Maconochie N, Davies G, Maconochie I, Pelerin M, Prior S, Lewis S (2004) Miscarriage, stillbirth and congenital malformation in the offspring of UK veterans of the first gulf war. Int J Epidemiol 33:74–86CrossRefGoogle Scholar
  15. 15.
    Al-Sadoon I, Hassan GG, Yacouba AA-H (1999) Depleted uranium and health of people in Basrah: epidemiological evidence. The incidence and pattern of congenital anomalies among births in Basrah during the period 1990-1998. MJBU 17:27–33Google Scholar
  16. 16.
    Fasy TM (2003) The recent epidemic of pediatric malignancies and congenital malformations in Iraq: the biological plausibility of depleted uranium as a carcinogen and a teratogen. In proceedings of the Iraqi-American Academics’ Symposium for Peace: 14-16 January 2003. BaghdadGoogle Scholar
  17. 17.
    Busby C, Hamdan M, Ariabi E (2010) Cancer, infant mortality and birth sex-ratio in Fallujah, Iraq 2005-2009. Int J Environ Res Public Health 7:2828–2837.  https://doi.org/10.3390/ijerph7072828 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Hagopian A, Lafta R, Hassan J, Davis S, Mirick D, Takaro T (2010) Trends in childhood leukemia in Basrah, Iraq, 1993-2007. Am J Public Health 100:1081–1087.  https://doi.org/10.2105/AJPH.2009.164236 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Al-Hadithi TS, Al-Diwan JK, Saleh AM, Shabila NP (2012) Birth defects in Iraq and the plausibility of environmental exposure: a review. 6(1):3. doi:  https://doi.org/10.1186/1752-1505-6-3 CrossRefGoogle Scholar
  20. 20.
    Marshall AC (2008) Gulf war depleted uranium risks. J Expo Sci Environ Epidemiol 18:95–108CrossRefGoogle Scholar
  21. 21.
    Iraq Ministry of Health (2013) Summary report on the congenital birth defects study in Iraq. http://www.emro.who.int/irq/iraq-news/summary-report-on-the-congenital-birth-defects-study-in-iraq.html
  22. 22.
    McDiarmid MA, Engelhardt SM, Dorsey CD, Oliver M, Gucer P, Gaitens JM, Kane R, Cernich A, Kaup B, Hoover D, Gaspari AA, Shvartsbeyn M, Brown L, Squibb KS (2011) Longitudinal health surveillance in a cohort of gulf war veterans 18 years after first exposure to depleted uranium. J Toxicol Environ Health A 74:678–691.  https://doi.org/10.1080/15287394.2011.539138 CrossRefPubMedGoogle Scholar
  23. 23.
    McDiarmid MA, Gaitens JM, Hines S, Breyer R, Wong-You-Cheong JJ, Engelhardt SM, Oliver M, Gucer P, Kane R, Cernich A, Kaup B, Hoover D, Gaspari AA, Liu J, Harberts E, Brown L, Centeno JA, Gray PJ, Xu H, Squibb KS (2013) The gulf war depleted uranium cohort at 20 years: bioassay results and novel approaches to fragment surveillance. Health Phys 104:347–361.  https://doi.org/10.1097/HP.0b013e31827b1740 CrossRefPubMedGoogle Scholar
  24. 24.
    McDiarmid MA, Gaitens JM, Hines S, Condon M, Roth T, Oliver M, Gucer P, Brown L, Centeno JA, Streeten E, Squibb KS (2015) Biologic monitoring and surveillance results for the Department of Veterans Affairs’ depleted uranium cohort: lessons learned from sustained exposure over two decades. AJIM 58:583–594.  https://doi.org/10.1002/ajim.22435 CrossRefGoogle Scholar
  25. 25.
    McDiarmid MA, Gaitens JM, Hines S, Condon M, Roth T, Oliver M, Gucer P, Brown L, Centeno JA, Dux M, Squibb KS (2017) The U.S. Department of Veterans’ affairs depleted uranium exposed cohort at 25 years: longitudinal surveillance results. Environ Res 152:175–184.  https://doi.org/10.1016/j.envres.2016.10.016 CrossRefPubMedGoogle Scholar
  26. 26.
    McDiarmid MA, Keogh JP, Hooper FJ, McPhaul K, Squibb K, Kane R, DiPino R, Kabat M, Kaup B, Anderson L, Hoover D, Brown L, Hamilton M, Jacobson-Kram D, Burrows B, Walsh M (2000) Health effects of depleted uranium on exposed gulf war veterans. Environ Res 82:168–180CrossRefGoogle Scholar
  27. 27.
    McDiarmid MA, Engelhardt S, Oliver M, Gucer P, Wilson PD, Kane R, Kabat M, Kaup B, Anderson L, Hoover D, Brown L, Handwerger B, Albertini RJ, Jacobson-Kram D, Thorne CD, Squibb KS (2004) Health effects of depleted uranium on exposed gulf war veterans: a 10-year follow-up. J Toxicol Environ Health A 67:277–296CrossRefGoogle Scholar
  28. 28.
    McDiarmid MA, Engelhardt SM, Dorsey CD, Oliver M, Gucer P, Wilson PD, Kane R, Cernich A, Kaup B, Anderson L, Hoover D, Brown L, Albertini R, Gudi R, Squibb KS (2009) Surveillance results of depleted uranium-exposed gulf war I veterans: sixteen years of follow-up. J Toxicol Environ Health A 72:14–29.  https://doi.org/10.1080/15287390802445400 CrossRefPubMedGoogle Scholar
  29. 29.
    McDiarmid MA, Squibb K, Engelhardt S, Oliver M, Gucer P, Wilson PD, Kane R, Kabat M, Kaup B, Anderson L, Hoover D, Brown L, Jacobson-Kram D (2001) Surveillance of depleted uranium exposed gulf war veterans: health effects observed in an enlarged “friendly fire” cohort. J Occup Environ Med 43:991–1000CrossRefGoogle Scholar
  30. 30.
    Ejnik JW, Hamilton MM, Adams PR, Carmichael AJ (2000) Optimal sample preparation conditions for the determination of uranium in biological samples by kinetic phosphorescence analysis (KPA). J Pharm Biomed Anal 15:227–235CrossRefGoogle Scholar
  31. 31.
    Gray PJ, Zhang L, Xu H, McDiarmid M, Squibb K, Centeno JA (2012) Determination of 236U/238U and 235U/238U isotope ratios in human urine by inductively coupled plasma mass spectrometry. Microchem J 105:94–100.  https://doi.org/10.1093/rpd/ncu023 CrossRefGoogle Scholar
  32. 32.
    Todorov TI, Xu H, Ejnik JW, Mullick FG, Squibb K, McDiarmid MA, Centeno J (2009) Depleted uranium analysis in blood by inductively coupled plasma mass spectrometry. J Anal At Spectrom 24:189–193CrossRefGoogle Scholar
  33. 33.
    Todorov TI, Ejnik JW, Guandalini G, Xu H, Hoover D, Anderson L, Squibb K, McDiarmid MA, Centeno JA (2013) Uranium quantification in semen by inductively coupled plasma mass spectrometry. J Trace Elem Med Biol 27:2–6.  https://doi.org/10.1016/j.jtemb.2012.07.004 CrossRefPubMedGoogle Scholar
  34. 34.
    Bertrand G, Vladesco R (1921) Intervention probable du zinc dans les phenomenes de fecundation chez les animaux vertebres. C.R. Acad Sci 173:176–179Google Scholar
  35. 35.
    Plechaty MM, Noll B, Sunderman FW (1977) Lead concentrations in semen of healthy men without occupational exposure to lead. Ann Clin Lab Sci 7:515–518PubMedGoogle Scholar
  36. 36.
    Lancranjan I, Popescu HI, Gavanescu O, Klepsch I, Serbanescu M (1975) Reproductive ability of workmen occupationally exposed to lead. Arch Environ Health 30:396–401CrossRefGoogle Scholar
  37. 37.
    Djordjevic M, Bunjevacki I (1966) Mass intoxication with ethylated gasoline. Proceedings 15th international congress on occupational health. Vienna Austria, Sept 19-24, Vol II-1:449–452Google Scholar
  38. 38.
    Monkiewicz J, Jaczewski S, Dynarowicz I (1975) Content of heavy metals in the semen of bulls from various environments. Med Weter 31:684–684Google Scholar
  39. 39.
    Pleban PA, Mei DS (1983) Trace elements in human seminal plasma and spermatozoa. Clin Chim Acta 133:43–50CrossRefGoogle Scholar
  40. 40.
    Saaranen M, Suistomaa U, Kantola M, Saarikoski S, Vanha-Perttula T (1987) Lead, magnesium, selenium and zinc in human seminal fluid: comparison with semen parameters and fertility. Hum Reprod 2:475–479CrossRefGoogle Scholar
  41. 41.
    Xu B, Chia SE, Tsakok M, Ong CN (1993) Trace elements in blood and seminal plasma and their relationship to sperm quality. Reprod Toxicol 7:613–618CrossRefGoogle Scholar
  42. 42.
    Apostoli P, Porru S, Morandi C, Menditto A (1997) Multiple determination of elements in human seminal plasma and spermatozoa. J Trace Elem Med Biol 11:182–184CrossRefGoogle Scholar
  43. 43.
    Hovatta O, Venäläinen ER, Kuusimäki L, Heikkilä J, Hirvi T, Reima I (1998) Aluminium, lead and cadmium concentrations in seminal plasma and spermatozoa, and semen quality in Finnish men. Hum Reprod 13:115–119CrossRefGoogle Scholar
  44. 44.
    Slivkova J, Popelkova M, Massanyi P, Toporcerova S, Stawarz R, Formicki G, Lukac N, Putała A, Guzik M (2009) Concentration of trace elements in human semen and relation to spermatozoa quality. J Environ Sci Health A Tox Hazard Subst Environ Eng 44:370–375.  https://doi.org/10.1080/10934520802659729 CrossRefPubMedGoogle Scholar
  45. 45.
    Khan PS, Skandhan KP, Ajesh K, Siraj MV (2011) Gold in human semen around and away from a gold deposit area. Biol Trace Elem Res 142:302–308.  https://doi.org/10.1007/s12011-010-8783-1 CrossRefGoogle Scholar
  46. 46.
    Mendiola J, Moreno JM, Roca M, Vergara-Juárez N, Martínez-García MJ, García-Sánchez A, Elvira-Rendueles B, Moreno-Grau S, López-Espín JJ, Ten J, Bernabeu R, Torres-Cantero AM (2011) Relationships between heavy metal concentrations in three different body fluids and male reproductive parameters: a pilot study. Environ Health 10(1):6.  https://doi.org/10.1186/1476-069X-10-6 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Li P, Zhong Y, Jiang X, Wang C, Zuo Z, Sha A (2012) Seminal plasma metals concentration with respect to semen quality. Biol Trace Elem Res 148:1–6.  https://doi.org/10.1007/s12011-012-9335-7 CrossRefPubMedGoogle Scholar
  48. 48.
    Mínguez-Alarcón L, Mendiola J, Roca M, López-Espín JJ, Guillén JJ, Moreno JM, Moreno-Grau S, Martínez-García MJ, Vergara-Juárez N, Elvira-Rendueles B, García-Sánchez A, Ten J, Bernabeu R, Torres-Cantero AM (2012) Correlations between different heavy metals in diverse body fluids: studies of human semen quality. Adv Urol 2012:1–11.  https://doi.org/10.1155/2012/420893 CrossRefGoogle Scholar
  49. 49.
    Giaccio L, Cicchella D, De Vivo B, Lombardi G, De Rosa M (2012) Does heavy metals pollution affects semen quality in men? A case of study in the metropolitan area of Naples (Italy). J Geochem Explor 112:218–225CrossRefGoogle Scholar
  50. 50.
    Thun MJ, Baker DB, Steenland K, Smith AB, Halperin W, Berl T (1985) Renaltoxicity in uranium mill workers. Scand J Work Environ Health 11:83–90CrossRefGoogle Scholar
  51. 51.
    Estaban M, Castaño A (2009) Non-invasive matrices in human biomonitoring: a review. Environ Int 35:438–449.  https://doi.org/10.1016/j.envint.2008.09.003 CrossRefGoogle Scholar
  52. 52.
    Ejnik JW, Todorov TI, Mullick FG, Squibb K, McDiarmid MA, Centeno JA (2005) Uranium analysis in urine by inductively coupled plasma dynamic reaction cell mass spectrometry. Anal Bioanal Chem 382:73–79.  https://doi.org/10.1007/s00216-005-3173-9 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Melissa A. McDiarmid
    • 1
    • 2
  • Patricia Gucer
    • 1
    • 2
  • Jose A. Centeno
    • 3
  • Todor Todorov
    • 3
  • Katherine S. Squibb
    • 1
    • 2
  1. 1.Department of Veterans Affairs Medical Center BaltimoreBaltimoreUSA
  2. 2.Department of MedicineUniversity of Maryland School of MedicineBaltimoreUSA
  3. 3.Center for Devices and Radiological Health Office of Science and Engineering LaboratoriesUS Food and Drug AdministrationSilver SpringUSA

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