Skip to main content

Distribution of serum levels of persistent organic pollutants, heterocyclic aromatic amine theoretical intake and nutritional cofactors in a semi-rural island population

Abstract

Persistent organic pollutant (POP) exposure is strongly associated with negative health effects in humans. Heterocyclic aromatic amines (HAAs) are formed during high temperature cooking of foods (i.e. meat and fish). Human exposure to HAA is through food consumption and from similar food groups to POPs. A study of serum samples for POPs in a non-occupational exposed population (n = 149, age range 18–80 years, recruited in 2012) and comparison with estimated HAA daily intake calculations based on food diaries were undertaken. Three different age groups (group 1, 18–29 years; group 2, 30–44 years; and group 3, 45–80 years) were used to explore possible relationships between POP levels present in blood, HAA intake and nutritional cofactors. Significant differences (p < 0.05) between groups (1 and 3) for POP levels were found for p,p′-DDE, polychlorinated biphenyl (PCB) 153, PCB 138 and the sum of PCBs. A similar trend was found between groups 2 and 3 for PCB 153 and sum of PCBs. Significant differences were found between groups 1 and 3 and groups 2 and 3 for HAA intake., i.e. HAA intake was lowest in those of middle age, which may well reflect a different pathway of human exposure between HAA and POPs through the diet preferences.

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

Fig. 1
Fig. 2
Fig. 3

Abbreviations

POPs:

Persistent organic pollutants

HAAs:

Heterocyclic aromatic amines

UNEP:

United Nations Environment Program

PCBs:

Polychlorinated biphenyls

p,p′-DDT:

p,p′-Dichlorodiphenyltrichloroethane

p,p′-DDD:

p,p′-Dichlorodiphenyldichloroethane

p,p′-DDE:

p,p′-Dichlorodiphenyldichloroethylene

HCB:

Hexachlorobenzene

HCH:

Hexachlorocyclohexane

ATSDR:

Agency for toxic substances and disease control

IARC:

International agency for research on cancer

OCs:

Organochlorine pesticides

BMI:

Body mass index

CHARRED:

Computerized heterocyclic amines resource for research in epidemiology of disease

LOD:

Lower limit of detection

LOQ:

Lower limit of quantification

GC-MS:

Gas chromatography/mass spectrometry

References

  • Aaslyng MD, Duedahl-Olesen L, Jensen K, Meinert L (2012) Content of heterocyclic amines and polycyclic aromatic hydrocarbons in pork, beef and chicken barbecued at home by Danish consumers. Meat Sci 93:85–91

    Article  Google Scholar 

  • Agency for Toxic Substances and Disease Control (2015) United States Department of Health and Human Services http://www.atsdr.cdc.gov/toxfaqs/index.asp

  • Alaejos MS, Afonso AM (2011) Factors that affect the content of heterocyclic aromatic amines in foods. Compr Rev Food Sci F 10:52–108

    CAS  Article  Google Scholar 

  • Álvarez-Pedrerol M, Ribas-Fitó N, Torrent M, Carrizo D, Garcia-Esteban R, Grimalt JO, Sunyer J (2008) Thyroid disruption at birth due to prenatal exposure to β-hexachlorocyclohexane. Environ Int 34:737–740

    Article  Google Scholar 

  • Amodio E, Turci R, Massenti MF, Di Gaudio F, Minoia C, Vitale F et al (2012) Serum concentrations of persistent organic pollutants (POPs) in the inhabitants of a Sicilian city. Chemosphere 89:970–974

    CAS  Article  Google Scholar 

  • Aylward LL, Green E, Porta M, Maree-Toms L, Hond ED, Schulz C et al (2014) Population variation in biomonitoring data for persistent organic pollutants (POPs): an examination of multiple population-based datasets for application to Australian pooled biomonitoring data. Environ Int 68:127–138

    CAS  Article  Google Scholar 

  • Bergman A, Heindel JJ, Jobling S, Kidd KA, Zoeller RT. editors. State of the science of endocrine disrupting chemicals—2012. Geneva: United Nations Environment Programme and the World Health Organization; 2013. [Available: http://www.who. int/ceh/publications/endocrine/en/index.html [accessed 9 September 2015]

  • Carrizo D, Grimalt JO, Ribas-Fito N, Sunyer J, Torrent M (2006) Physical-chemical and maternal determinants of accumulation of organochlorine compounds in four-year-old children. Environ Sci Technol 40:1420–1426

    CAS  Article  Google Scholar 

  • Carrizo D, Grimalt JO, Ribas-Fito N, Sunyer J, Torrent M (2007) Influence of breastfeeding in the accumulation of polybromodiphenyl ethers during the first years of child growth. Environ Sci Technol 41:4907–4912

    CAS  Article  Google Scholar 

  • Carrizo D, Gustafsson O (2011a) Distribution and inventory of polychlorinated biphenyls in the polar mixed layer of the seven pan-Arctic shelf seas and interior basin. Environ Sci Technol 45:1420–1427

    CAS  Article  Google Scholar 

  • Carrizo D, Gustafsson O (2011b) Pan-Arctic river fluxes of polychlorinated biphenyls. Environ Sci Technol 45:8377–8384

    CAS  Article  Google Scholar 

  • Carpenter DO (2006) Polychlorinated biphenyls (PCBs): routes of exposure and effects on human health. Rev Environ Health 21:1–23

    CAS  Article  Google Scholar 

  • Chang S-H, Moss BW, Farmer LJ, Gordon A, Cuskelly GJ (2013) Comparison of consumer perception and acceptability for steaks cooked to different endpoints: validation of photographic approach. Food Chem 136:1597–1602

    Article  Google Scholar 

  • Cheng K, Chen F, Wang M (2006) Heterocyclic amines: chemistry and health. Mol Nutr Food Res 50:1150–1170

    CAS  Article  Google Scholar 

  • de Wit CA, Alaee M, Muir DC (2006) Levels and trends of brominated flame retardants in the Arctic. Chemosphere 64:209–233

    Article  Google Scholar 

  • Fitt E, Prynne CJ, Teucher B, Swan G, Stephen AM (2009) National diet and nutrition survey: assigning mixed dishes to food groups in the nutrient databank. J Food Compos Anal 22:S52–S56

    Article  Google Scholar 

  • Grimalt JO, Howsam M, Carrizo D, Otero R, Rodrigues de Marchi MR, Vizcaino E (2010) Integrated analysis of halogenated organic pollutants in sub-millilitre volumes of venous and umbilical cord blood sera. Anal Bioanal Chem 396:2265–2272

    CAS  Article  Google Scholar 

  • Health Canada (2002) Consumption advice: making informed choices about fish Available: http://www.hc-sc.gc.ca/fn-an/securit/che​m-chim/environ/mercur/cons-adv-etud-eng.​php accessed 8 December 2010

  • International Agency for Research on Cancer (1993a) Some natural occurring and synthetic food components, furocoumarins and ultraviolet radiation. IARC Monographs of the Evaluation of the Carcinogenic Risk of Chemicals to Humans 56:165–195

    Google Scholar 

  • International Agency for Research on Cancer (2015) Volume 114: Consumption of red meat and processed meat. IARC Working Group. Lyon; 6–13 September, 2015. IARC Monogr Eval Carcinog Risks Hum (in press)

  • International Agency for Research on Cancer (1993b) Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. IARC Monographs of the Evaluation of the Carcinogenic Risk of Chemicals to Humans 56:196–242

    Google Scholar 

  • Lam TK, Cross AJ, Consonni D, Randi G, Bagnardi V, Bertazzi PA et al (2009) Intakes of red meat, processed meat, and meat mutagens increase lung cancer risk. Cancer Res 69:932–939

    CAS  Article  Google Scholar 

  • Nelson M, Atkinson M, Meyer J (2002) Food portion sizes: a photographic atlas, 3rd edn. Food Standards Agency, MAFF Publications, London

    Google Scholar 

  • Orta-García S, Perez-Vazquez F, Gonzalez-Vega C, Varela-Silva JA, Hernandez-Gonzalez L, Perez-Maldonado I (2014) Concentrations of persistent organic pollutants (POPs) in human blood samples from Mexico City, Mexico. Sci Tot Env 472:496–501

    Article  Google Scholar 

  • Porta M, Pumarega J, Gasull M (2012) Number of persistent organic pollutants detected at high concentrations in a general population. Environ Int 44:106–111

    CAS  Article  Google Scholar 

  • Porta M, Gasull M, Puigdomenech E, Gari M, Bosch de Basea M et al (2010) Distribution of blood concentrations of persistent organic pollutants in a representative sample of the population of Catalonia. Environ Int 36:655–664

    CAS  Article  Google Scholar 

  • Puangsombat K, Gadgil P, Houser TA, Hunt MC, Smith JS (2012) Occurrence of heterocyclic amines in cooked meat products. Meat Sci 90:739–746

    CAS  Article  Google Scholar 

  • Quinn CL, Wania F (2012) Understanding differences in the body burden-age relationships of bioaccumulating contaminants based on population cross sections versus individuals. Environ Health Perspect 120:554–559

    CAS  Article  Google Scholar 

  • Rohrmann S, Zoller D, Hermann S, Linseisen J (2007) Intake of heterocyclic aromatic amines from meat in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Heildelberg cohort. Br J Nutr 98:1112–1115

    CAS  Article  Google Scholar 

  • Schecter A, Colacino J, Haffner D et al (2010) Perfluorinated compounds, polychlorinated biphenyls, and organochlorine pesticide contamination in composite food samples from Dallas, Texas, USA. Environ Health Perspect 118:796–802

    CAS  Article  Google Scholar 

  • Sinha R, Knize MG, Salmon CP, Brown ED, Rhodes D, Felton JS et al (1998a) Heterocyclic amine content of pork products cooked by different methods and to varying degrees of doneness. Food Chem Toxicol 36:289–297

    CAS  Article  Google Scholar 

  • Sinha R, Rothman N, Salmon CP, Knize MG, Brown DE, Swanson CA et al (1998b) Heterocyclic amine content in beef cooked by different methods to varying degrees of doneness and gravy made from meat drippings. Food Chem Toxicol 36:279–287

    CAS  Article  Google Scholar 

  • Sinha R (2002) An epidemiologic approach to studying heterocyclic amines. Mutant Res Fund Mol M 506:197–204

    Article  Google Scholar 

  • Sugimura T, Wakabayashi K, Nakagama H, Nagao M (2004) Heterocyclic amines: mutagens/carcinogens produced during cooking of meat and fish. Cancer Sci 95:290–299

    CAS  Article  Google Scholar 

  • Sperry WM (1995) Lipid analysis: methods of biochemical analysis (vol. 2), Glick, D. Ed. Interscience, New York, p 83

    Google Scholar 

  • Strøm M, Hansen S, Fróði Olsen S, Småstuen Haug L, Rantakokko P, Kiviranta H et al (2014) Persistent organic pollutants measured in maternal serum and offspring neurodevelopmental outcomes—a prospective study with long-term follow-up. Environ Int 68:41–48

    Article  Google Scholar 

  • Szterk A (2015) Heterocyclic aromatic amines in grilled beef: the influence of free amino acids, nitrogenous bases, nucleosides, protein and glucose on HAAs content. J Food Compos Anal 40:39–46

    CAS  Article  Google Scholar 

  • Tang D, Kryvenko ON, Wang Y, Trudeau S, Rundle A, Takahashi S et al (2013) 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP)-DNA adducts in benign prostate and subsequent risk for prostate cancer. Int J Cancer 133:961–971

    CAS  Article  Google Scholar 

  • Turyk ME, Bhavsar SP, Bowerman W, Boysen E, Clark M, Diamond M et al (2012) Risks and benefits of consumption of Great Lakes fish. Environ Health Perspect 120:11–18

    CAS  Article  Google Scholar 

  • UNEP. United Nations Environment Programme (2011) Stockholm convention on persistent organic pollutants (POPs). Geneva, Switzerland: Text and annexes; [20011–64 Available from: www.unep.org]

  • US National Cancer Institute. CHARRED database [Online] (2015) Computerized heterocyclic amines rsource for research in epidemiology of disease Available at: http://dceg.cancer.gov/tools/design/charred Accessed on 23 April 2015

  • Warzecha L, Janoszka B, Blaszczyk U, Strozyk M, Bodzek D, Dobosz C (2004) Determination of heterocyclic aromatic amines (HAs) content in samples of household-prepared meat dishes. J of Chromatography B 802:95–106

    CAS  Article  Google Scholar 

  • Withehead TP, Crispo Smith S, June-Soo P, Petreas MX, Rappaport SM, Metayer C (2015) Concentrations of persistent organic pollutants in California women’s serum and residential dust. Environ Res 136:57–66

    Article  Google Scholar 

  • Zhang Y, Yu C, Mei J, Wang S (2013) Formation and mitigation of heterocyclic aromatic amines in fried pork. Food Addit Contam A: Chem Anal Control Expo Risk Assess 30:1501–1507

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was supported by The World Cancer Research Fund. D. Carrizo acknowledges Ministerio de Economía y Competitividad (Spain) for the financial support through a Ramón y Cajal (RYC) Contract (RYC-2014-19446).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel Carrizo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Roland Kallenborn

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Carrizo, D., Brennan, S.F., Chevallier, O.P. et al. Distribution of serum levels of persistent organic pollutants, heterocyclic aromatic amine theoretical intake and nutritional cofactors in a semi-rural island population. Environ Sci Pollut Res 24, 22393–22401 (2017). https://doi.org/10.1007/s11356-017-9851-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-9851-2

Keywords

  • POPs
  • HAA
  • Estimated daily intake
  • Human exposure
  • Food diaries
  • Nutritional cofactors