Skip to main content
Log in

Sperm DNA damage correlates with polycyclic aromatic hydrocarbons biomarker in coke-oven workers

  • Original Article
  • Published:
International Archives of Occupational and Environmental Health Aims and scope Submit manuscript

Abstract

Objectives: The aim was to determine whether occupational exposure to polycyclic aromatic hydrocarbons (PAHs) in men has adverse effect on semen quality. Methods: Forty-eight coke-oven workers, including 16 topside-oven (TO) workers and 32 sideoven (SO) workers, were studied. Ambient PAHs exposure, urinary 1-hydroxypyrene (1-OHP) levels, and parameters of semen quality were determined. Results: TO workers had significantly higher ambient PAHs exposure (3,436.1±3,411.0 vs. 1,123.1±1,829.3 ng/m3, P<0.01), urinary 1-OHP levels (207.8±176.4 vs. 54.0±44.8 μg/g, P<0.001), frequency of oligospermia (18.8 vs. 0%, P<0.05), and morphological abnormality in sperm (32.3 vs. 14.6%, P<0.01) than SO workers. Among cigarette smokers, TO workers had significantly higher rates of DNA denaturation in spermatozoa (αT) and percentage of sperm with increased DNA denaturation (COMP αT) levels than SO workers (246.2±49.5 vs. 198.1±30.3 for αT; 34.8±14.4 vs. 19.3±13.9% for COMP αT, P<0.05). There was a positive correlation between urinary 1-OHP and αT, COMP αT, and abnormal sperm morphology and a tenfold increase in urinary 1-OHP associated with a 2.35-fold increase in αT, as well as a 1.07-fold increase in percentage of sperm with abnormal morphology. Conclusions: A potential risk of sperm dysfunction should be considered for workers occupationally exposed to high levels of PAHs. Cigarette smoking may aggravate this risk. Urinary 1-OHP can be used as a biomarker predicting sperm dysfunction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

1-OHP:

1-Hydroxypyrene

BaP:

Benzo(a)pyrene

COMP αT:

Cells falling outside of the main population

αT:

DNA denaturation per spermatozoa

FCM:

Flow cytometry

MMP:

Mitochondrial membrane potential

NS:

Non-smoking

PAHs:

Polycyclic aromatic hydrocarbons

SO:

Sideoven

SM:

Smoking

TO:

Topside-oven

References

  • Armstrong B, Hutchinson E, Unwin J, Fletcher T (2004) Lung cancer risk after exposure to polycyclic aromatic hydrocarbons: a review and meta-analysis. Environ Health Perspect 112:970–978

    PubMed  CAS  Google Scholar 

  • Auger J, Kunstman JM, Czyglik F, Jouannet P (1995) Decline in semen quality among fertile men in Paris during the past 20 years. N Engl J Med 332:281–285

    Article  PubMed  CAS  Google Scholar 

  • Boogaard PJ, Sittert NJ (1994) Exposure to polycyclic aromatic hydrocarbons in petrochemical industries by measurement of urinary 1-hydroxypyrene. Occup Environ Med 51:250–258

    PubMed  CAS  Google Scholar 

  • Boogaard PJ, Sittert NJ (1995) Urinary 1-hydroxypyrene as biomarker of exposure to polycyclic aromatic hydrocarbons in workers in petrochemical industries: baseline values and dermal uptake. Sci Total Environ 163:203–209

    Article  PubMed  CAS  Google Scholar 

  • Bouchard M, Thuot T, Carrier G, Viau C (2002) Urinary excretion kinetics of 1-hydroxypyrene in rats subchronically exposed to pyrene or polycyclic aromatic hydrocarbon mixtures. J Toxicol Environ Health A 65:1195–1209

    Article  PubMed  CAS  Google Scholar 

  • Chen ML, Mao IF, Wu MT, Chen JR, Ho CK, Smith TJ, Wypij D, Christiani DC (1999) Assessment of coke oven emissions exposure among coking workers. Am Ind Hyg Assoc J 60:105–110

    PubMed  CAS  Google Scholar 

  • Chia SE, Xu B, Ong CN, Tsakok FM, Lee ST (1994) Effect of cadmium and cigarette smoking on human semen quality. Int J Fertil Menopausal Stud 39:292–298

    PubMed  CAS  Google Scholar 

  • Dunphy BC, Barratt CL, von Tongelen BP, Cooke ID (1991) Male cigarette smoking and fecundity in couples attending an infertility clinic. Andrologia 23:223–225

    Article  PubMed  CAS  Google Scholar 

  • Evenson DP, Jost LK, Baer RK, Turner TW, Schrader SM (1991) Individuality of DNA denaturation patterns in human sperm as measured by the sperm chromatin structure assay. Reprod Toxicol 5:115–125

    Article  PubMed  CAS  Google Scholar 

  • Gaspari L, Chang SS, Santella RM, Garte S, Pedotti P, Taioli E (2003) Polycyclic aromatic hydrocarbon-DNA adducts in human sperm as a marker of DNA damage and infertility. Mutat Res 535:155–160

    PubMed  CAS  Google Scholar 

  • Hatjian BJ, Edwards JW, Harrison J, Williams FM, Blain PG (1995) Ambient, biological, and biological effect monitoring of exposure to polycyclic aromatic hydrocarbons (PAHs). Toxicol Lett 77:271–279

    Article  PubMed  CAS  Google Scholar 

  • Hu CW, Wu MT, Chao MR, Pan CH, Wang CJ, Swenberg JA, Wu KY (2004) Comparison of analyses of urinary 8-hydroxy-2′-deoxyguanosine using isotope-dilution liquid chromatography electrospray tandem mass spectrometry and enzyme-linked immunosorbent assay. Rapid Commun Mass Spectrom 18:505–510

    Article  PubMed  CAS  Google Scholar 

  • International Agency for Research on Cancer (1984) IARC monograph on the evaluation of carcinogenic risks to humans. Polynuclear aromatic compounds. Part 3. Industrial exposures in aluminum production, coal gasification, coke production, and iron and steel founding. IARC, Lyon

  • Inyang F, Ramesh A, Kopsombut P, Niaz MS, Hood DB, Nyanda AM, Archibong AE (2003) Disruption of testicular steroidogenesis and epididymal function by inhaled benzo(a)pyrene. Reprod Toxicol 17:527–537

    Article  PubMed  CAS  Google Scholar 

  • Jongeneelen FJ (1992) Biological exposure limit for occupational exposure to coal tar pitch volatiles at cokeovens. Int Arch Occup Environ Health 63:511–516

    Article  PubMed  CAS  Google Scholar 

  • Kalcher K, Kern W, Pietsch R (1993) Cadmium and lead in the smoke of a filter cigarette. Sci Total Environ 128:21–35

    Article  PubMed  CAS  Google Scholar 

  • Kang DH, Rothman N, Poirier MC, Greenberg A, Hsu CH, Schwartz BS, Baser ME, Groopman JD (1995) Interindividual differences in the concentration of 1-hydroxypyrene-glucuronide in urine and polycyclic aromatic hydrocarbon-DNA adducts in peripheral white blood cells after charbroiled beef consumption. Carcinogenesis 16:1079–1085

    Article  PubMed  CAS  Google Scholar 

  • Keimig SD, Kirby KW, Morgan DP, Keiser JE, Hubert TD (1983) Identification of 1-hydroxypyrene as a major metabolite of pyrene in pig urine. Xenobiotica 13:415–420

    Article  PubMed  CAS  Google Scholar 

  • Khorram O, Garthwaite M, Jones J, Golos T (2004) Expression of aryl hydrocarbon receptor (AHR) and aryl hydrocarbon receptor nuclear translocator (ARNT) mRNA expression in human spermatozoa. Med Sci Monit 10:BR135–BR138

    PubMed  CAS  Google Scholar 

  • Marczynski B, Preuss R, Mensing T, Angerer J, Seidel A, El Mourabit A, Wilhelm M, Bruning T (2005) Genotoxic risk assessment in white blood cells of occupationally exposed workers before and after alteration of the polycyclic aromatic hydrocarbon (PAH) profile in the production material: comparison with PAH air and urinary metabolite levels. Int Arch Occup Environ Health 78:97–108

    Article  PubMed  CAS  Google Scholar 

  • Ny ET, Heederik D, Kromhout H, Jongeneelen FJ (1993) The relationship between polycyclic aromatic hydrocarbons in air and in urine of workers in a Soderberg potroom. Am Ind Hyg Assoc J 54:277–284

    PubMed  CAS  Google Scholar 

  • Pacifici R, Altieri I, Gandini L, Lenzi A, Pichini S, Rosa M, Zuccaro P, Dondero F (1993) Nicotine, cotinine, and trans-3-hydroxycotinine levels in seminal plasma of smokers: effects on sperm parameters. Ther Drug Monit 15:358–363

    Article  PubMed  CAS  Google Scholar 

  • Paracchini V, Chang S-S, Santella RM, Garte S, Pedotti P, Taioli E (2005) GSMT1 deletion modifies the levels of polycyclic aromatic hydrocarbon–DNA adducts in human sperm. Mutat Res 586:97–101

    PubMed  CAS  Google Scholar 

  • Paulozzi LJ, Erickson D, Jackson RJ (1997) Hypospadias trends in two US surveillance systems. Pediatrics 10:831–834

    Article  Google Scholar 

  • Ramesh A, Inyang F, Hood DB, Archibong AE, Knuckles ME, Nyanda AM (2001) Metabolism, bioavailability, and toxicokinetics of benzo(a)pyrene in F-344 rats following oral administration. Exp Toxicol Pathol 53:275–290

    Article  PubMed  CAS  Google Scholar 

  • Revel A, Raanani H, Younglai E, Xu J, Han R, Savouret J-F, Casper RF (2001) Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects sperm from DNA damage and apoptosis caused by benzo(a)pyrene. Reprod Toxicol 15:479–486

    Article  PubMed  CAS  Google Scholar 

  • Seleven SG, Borkovec L, Slott VL, Zudova Z, Rubes J, Evenson DP (2000) Semen quality and reproductive health of young Czech men exposed to seasonal air pollution. Environ Health Perspect 108:887–894

    Article  PubMed  Google Scholar 

  • Shen HM, Chia SE, Ni ZY, New AL, Lee BL, Ong CN (1997) Detection of oxidative DNA damage in human sperm and association with cigarette smoking. Reprod Toxicol 11:675–680

    Article  PubMed  CAS  Google Scholar 

  • Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, Steele GD Jr, Chen LB (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci USA 88:3671–3675

    Article  PubMed  CAS  Google Scholar 

  • Sram RJ, Binkova B, Rossner P, Rubes J, Topinka J, Dejmek J (1999) Adverse reproductive outcomes from exposure to environmental mutagens. Mutat Res 428:203–215

    PubMed  CAS  Google Scholar 

  • Tas S, Lauwerys R, Lison D (1996) Occupational hazards for the male reproductive system. Crit Rev Toxicol 26:261–307

    Article  PubMed  CAS  Google Scholar 

  • Tsai PJ, Shieh HY, Lee WJ, Chen HL, Shih TS (2002) Urinary 1-hydroxypyrene as a biomarker of internal dose of polycyclic aromatic hydrocarbons in carbon black workers. Ann Occup Hyg 46:229–235

    Article  PubMed  CAS  Google Scholar 

  • Vinggaard AM, Hnida C, Larsen JC (2000) Environmental polycyclic aromatic hydrocarbons affect androgen receptor activation in vitro. Toxicology 145:173–183

    Article  PubMed  CAS  Google Scholar 

  • Wallock LM, Tamura T, Mayr CA, Johnston KE, Ames BN, Jacob RA (2001) Low seminal plasma folate concentrations are associated with low sperm density and count in male smokers and nonsmokers. Fertil Steril 75:252–259

    Article  PubMed  CAS  Google Scholar 

  • Wang SL, Wang XR, Chia SE, Shen HM, Song L, Xing HX, Chen HY, Ong CN (2001) A study on occupational exposure to petrochemicals and smoking on seminal quality. J Androl 22:73–78

    PubMed  Google Scholar 

  • World Health Organization (2002) WHO laboratory manual for the examination of human semen and seminal–cervical mucus interaction, 3rd edn. WHO, Cambridge University Press, Cambridge

    Google Scholar 

  • Wu MT (2002) Assessment of the effectiveness of respirator usage in coke oven workers. AIHA J 63:72–75

    Article  CAS  Google Scholar 

  • Wu MT, Kelsey KT, Mao IF, Wypij D, Christiani DC (1997) Elevated serum liver enzymes in coke oven and by-product workers. J Occup Environ Med 39:527–533

    Article  PubMed  CAS  Google Scholar 

  • Wu MT, Mao IF, Ho CK, Wypij D, Lu PL, Smith TJ, Chen ML, Christiani DC (1998) Urinary 1-hydroxypyrene concentrations in coke oven workers. Occup Environ Med 55:461–467

    Article  PubMed  CAS  Google Scholar 

  • Wu MT, Pan CH, Huang YL, Tsai PJ, Chen CJ, Wu TN (2003) Urinary excretion of 8-hydroxy-2-deoxyguanosine and 1-hydroxypyrene in coke-oven workers. Environ Mol Mutagen 42:98–105

    Article  PubMed  CAS  Google Scholar 

  • Zitzmann M, Rolf C, Nordhoff V, Schrader G, Rickert-Fohring M, Gassner P, Behre HM, Greb RR, Kiesel L, Nieschlag (2003) Male smokers have a decreased success rate for in vitro fertilization and intracytoplasmic sperm injection. Fertil Steril 79:1550–1554

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was funded by grants from the National Science Council of Taiwan (NSC 92-2320-B-327-001 to PCH) and from the Institute of Occupational Safety and Health Council of Labor Affairs, Taipei (IOSH93-M366 to MTW).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ming-Tsang Wu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hsu, PC., Chen, IY., Pan, CH. et al. Sperm DNA damage correlates with polycyclic aromatic hydrocarbons biomarker in coke-oven workers. Int Arch Occup Environ Health 79, 349–356 (2006). https://doi.org/10.1007/s00420-005-0066-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00420-005-0066-3

Keywords

Navigation