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Biomarkers of PAH exposure and hematologic effects in subjects exposed to combustion emission during residential (and professional) cooking practices in Pakistan

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Abstract

The aim of this study was to evaluate and compare the exposure of household women and professional male workers to combustion emission in the indoor and semi-outdoor environments, respectively, by using biochemical parameters and the biomarkers of exposure to polycyclic aromatic hydrocarbon (PAH). Female (WR n = 60) and male “cooks” (WC n = 60) exposed to the combustion emission of fuel wood and coal in rural/suburban areas of Pakistan were recruited in this study and compared to non-exposed female (CF) and male (CM) groups (n = 32 and 34, respectively). Urinary biomarkers of PAH exposure including 1-hyroxypyrene (1-OHPyr), α-naphthol, and β-naphthol were analyzed together with the biomarkers of effect, including the serum c-reactive proteins (CRP), white blood cells (WBCs), hemoglobin (Hb), red blood cells (RBC), and platelet (PLT) count. In addition, blood superoxide dismutase (SOD) and urinary level of 8-hydroxydeoxyguanosine (8-OHdG) were evaluated to determine the oxidative stress and DNA damage, respectively. A questionnaire was used to document demographic-, health-, and exposure-related information. The results showed that urinary β-naphthol was almost 44 % higher in WR subjects than WC (median 7.69 vs. 3.39 μmol/mol-Cr, respectively; p = 0.01) and respective controls (CF). Higher urinary 8-OHdG were observed in WR (71.1 ng/mg-Cr) than WC (56.37 ng/mg-Cr) (p < 0.001), and lower life status and higher degree of headache were observed in WR than WC. In WCs, however, a low Hb and high WBC (8.29 × 103 μL−1, ranging between 6.1 and 10.6 × 103 μL−1) were observed in comparison with CM. The study shows that WC subjects used larger amount of fuel and were subjected to prolonged exposure. It was concluded that the role of ventilation is fundamental and WR were more exposed to PAHs despite the fact that WC spent more time in cooking (due to occupational requirement) than WR.

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Abbreviations

1-OHPyr:

1-hyroxypyrene

8-OHdG:

8-hyroxydeoxyguanosine

BMI:

body mass index

CRP:

c-reactive protein

CVD:

cardiovascular disease

WR:

female residential cooks

Hb:

hemoglobin

HPLC:

high-pressure liquid chromatography

IQR:

interquartile range

KMO:

Kaiser-Meyer-Olkin measure of sample adequacy

WC:

male professional cooks

MCV:

mean corpuscular volume

MW:

molecular weight

PAHs:

polycyclic aromatic hydrocarbons

PCA:

principal component analysis

PLTs:

platelets

RBCs:

red blood cells

SOD:

superoxide dismutase

WBCs:

white blood cells

μmol/mol-Cr:

micromole per mole creatinine

References

  • ACGIH (2010) Documentation for a recommended BEI of polycyclic aromatic hydro-carbons. ACGIH, Cincinatti

    Google Scholar 

  • Adetona O, Li Z, Sjödin A, Romanoff LC, Aguilar-Villalobos M, Needham LL, Hall DB, Cassidy BE, Naeher LP (2013) Biomonitoring of polycyclic aromatic hydrocarbon exposure in pregnant women in Trujillo, Peru—comparison of different fuel types used for cooking. Environ Int 53:1–8

    Article  CAS  Google Scholar 

  • Al-Malki AL, Rezq AM, Al-Saedy MH (2008) Effect of fire smoke on some biochemical parameters in firefighters of Saudi Arabia. J Occup Med Toxicol 3:33

    Article  Google Scholar 

  • Alshaarawy O, Zhu M, Ducatman A, Conway B, Andrewc ME (2013) Polycyclic aromatic hydrocarbon biomarkers and serum markers of inflammation. A positive association that is more evident in men. Environ Res 126:98–104

    Article  CAS  Google Scholar 

  • Apostolakis S, Vogiatzi K, Amanatidou V, Spandidos DA (2009) Interleukin 8 and cardiovascular disease. Cardiovasc Res 84:353–360

    Article  CAS  Google Scholar 

  • Banerjee M, Siddique S, Mukherjee S, Roychoudhury S, Dase P, Ray MR, Lahiri T (2012) Hematological, immunological, and cardiovascular changes in individuals residing in a polluted city of India: a study in Delhi. Intern J Hyg Environ Health 215:306–311

    Article  CAS  Google Scholar 

  • Benson WH, Dorough MW (1984) Comparative ester hydrolysis of carbaryl and ethiofencarb in four mammalian species. Pestic Biochem Physiol 21(2):199–206

    Article  CAS  Google Scholar 

  • BMM biological monitoring methods. Group Support Unit Room L. 2. 51 Health and Safety Laboratory Harpur Hill Buxton 2005; SK17 9JN www.hsl.gov.uk

  • Bouchard M, Pinsonneault L, Tremblay C, Weber JP (2001) Biological monitoring of environmental exposure to polycyclic aromatic hydrocarbons in subjects living in the vicinity of a creosote impregnation plant. Int Arch Occup Environ Health 74:505–513

    Article  CAS  Google Scholar 

  • Bravo CF, Curtis LR, Myers MS, Meador JP, Johnson LL, Buzitis J, Collier TK, Morrow JD, Laetz CA, Loge FJ, Arkoosh MR (2011) Biomarker responses and disease susceptibility in juvenile rainbow trout Oncorhynchus mykiss fed a high molecular weight PAH mixture. Environ Toxicol Chem 30(30):704–714

    Article  CAS  Google Scholar 

  • Brook RD, Franklin B, Cascio W, Hong Y, Howard G, Lipsett M, Luepker R, Mittleman M, Samet J, Smith SC Jr, Tager I (2004) Air pollution and car-diovascular disease: a statement for healthcare professionals from the expert panel on population and prevention science of the American Heart Association. Circulation 109:2655–2671

    Article  Google Scholar 

  • Buchet JP, Ferreira M Jr, Burrion JB, Leroy T, Kirsch-Volders M, Van Hummelen P, Jacques J, Cupers L, Delavignette JP, Lauwerys R (1995) Tumor markers in serum, polyamines and modified nucleosides in urine, and cytogenetic aberrations in lymphocytes of workers exposed to PAH. Am J Ind Med 27:523–543

  • Cavanagh JAE, Brown L, Trought K, Kingham S, Epton MJ (2007) Elevated concentrations of 1-hydroxypyrene in schoolchildren during winter in Christchurch, New Zealand. Sci Total Environ 374(1):51–59

    Article  CAS  Google Scholar 

  • Chetiyanukornkul T, Toriba A, Kamede T, Tang N, Hayakawa K (2006) Simultaneous determination of urinary hydroxylated metabolites of naphthalene, fluorene, phenanthrene, fluoranthene and pyrene as multiple biomarkers of exposure to polycyclic aromatic hydrocarbons. Anal Bioanal Chem 386(3):712–718

    Article  CAS  Google Scholar 

  • Colbeck I, Nazir ZA, Ali Z (2009) Characteristics of indoor/outdoor particulate pollution in urban and rural residential environment of Pakistan. Indoor Air 20(1):40–51

    Article  Google Scholar 

  • Cookson MR, Shaw PJ (1999) Oxidative stress and motor neurone disease. Brain Pathol 9:165ral r

    Article  Google Scholar 

  • Dimitrova MST, Tsinova V, Velcheva V (1994) Combined effect of zinc and lead on the hepatic superoxide dismutase–catalase system in carp (Cyprinus carpio). Comp Biochem Physiol C 108:43–46

    Google Scholar 

  • Ding J, Zhong J, Yang Y, Li B, Shen G, Su Y, Wang C, Li W, She H, Wang B, Wang R, Huang Y, Zhang Y, Cao H, Zhu Y, Simonich SLM, Tao S (2012) Occurrence and exposure to polycyclic aromatic hydrocarbons and their derivatives in a rural Chinese home through biomass fuelled cooking. Environ Pollut 169:160–166

    Article  CAS  Google Scholar 

  • Dutta A, Bhattacharya P, Lahiri T, Ray MR (2012a) Immune cells and cardio-vascular health in premenopausal women of rural India chronically exposed to biomass smoke during daily household cooking. Sci Total Environ 438:293–298

    Article  CAS  Google Scholar 

  • Dutta A, Ray MR, Banerjee A (2012b) Systemic inflammatory changes and increased oxidative stress in rural Indian women cooking with biomass fuels. Toxicol Appl Pharmacol 261:255–262

    Article  CAS  Google Scholar 

  • Dutta A, Ray MR (2013) Increased cardiovascular risk due to systemic inflammatory changes and enhanced oxidative stress in urban Indian women. Air Qual Atmos Health 6:501–508

    Article  Google Scholar 

  • Ekici A, Eikici M, Kurtipek E, Akin A, Arslan M, Kara T (2005) Obstructive airway diseases in women exposed to biomass smoke. Environ Res 99:93–98

    Article  CAS  Google Scholar 

  • Elovaara E, Mikkola J, Makela M, Paldanius B, Priha E (2006) Assessment of soil remediation workers’ exposure to polycyclic aromatic hydrocarbons PAH: biomonitoring of naphthols phenanthrols and 1, hydroxypyrene in urine. Toxicol Lett 162(2,3):158–163

    Article  CAS  Google Scholar 

  • Everett CJ, King DE, Player MS, Matheson EM, Post RE, Mainous AG 3rd (2010) Association of urinary polycyclic aromatic hydrocarbons and serum C-reactive protein. Environ Res 110:79–82

    Article  CAS  Google Scholar 

  • Ezzati M, Kammen D (2001) Indoor air pollution from biomass combustion and acute respiratory infections in Kenya: an exposure-response study. Lancet 358:619–624

    Article  CAS  Google Scholar 

  • Giannapas M, Karnis L, Dailianis S (2011) Generation of free radicals in haemocytes of mussels after exposure to low molecular weight PAH components: immune activation, oxidative and genotoxic effects. Comparative biochemistry and physiology. Toxicol Pharmacol CBP 155(2):182–189

    Google Scholar 

  • Ha M, Kwon H, Cheong H-K, Lim S, Yoo SJ, Kim EJ, Park SG, Lee J, Chung BC (2012) Urinary metabolites before and after cleanup and subjective symptoms in volunteer participants in cleanup of the Hebei Spirit oil spill. Sci Total Environ 429:167–173

    Article  CAS  Google Scholar 

  • Hansen AM, Mathiesen L, Pedersen M, Knudsen LE (2008) Urinary 1-hydroxypyrene 1-HP in environmental and occupational studies, a review. Int J Hyg Environ Health 211(5, 6):471–503

  • Harijan K, Mohammad AU (2013) Potential of biomass conservation through dissemination of efficient cook stoves in Pakistan. APCBEE Procedia 5:358–362

    Article  Google Scholar 

  • HEI (2010) Health effects institute, traffic-related air pollution, a critical review of the literature on emissions, exposure, and health effects health effects institute. http://pubs.healtheffects.org/view.php?id=334

  • Hill RH, Head SL, Baker SE, Gregg M, Shealy DB, Bailey SL, Williams CC, Sampson EJ, Needham LL (1995) Pesticide residues in urine of adults living in the United States: reference range concentrations. Environ Res 71:99–108

    Article  CAS  Google Scholar 

  • Hirayama M, Nakamura T, Watanabe H, Uchida K, Hama T, Hara T, Niimi Y, Ito M, Ohno K, Sobue G (2011) Urinary 8-hydroxydeoxyguanosine correlate with hallucinations rather than motor symptoms in Parkinson’s disease. Parkinsonism Relat Disord 17:46–49

    Article  Google Scholar 

  • Holzer J, Wilhelm M (2007) A personel communication reported by Wilhelm M, Hardt J, Schulz C, Angerer J (2011) New reference value and the background exposure for the PAH metabolites 1-hydroxypyrene and 1- and 2-naphthol in urine of the general population in Germany: basis for validation of human biomonitoring data in environmental medicine Wood-Kaczmar A, Gandhi S, Wood NW. Trends Mol Med 12(11):521–528

  • HSE EH40/2011 (2011) Workplace exposure limits. HSE Books

  • IARC (2010a) Household use of solid fuels and high-temperature frying. IARC Monographs on the evaluation of carcinogenic risks to humans. Lyon: Intl Agency for Res Cancer 95

  • IARC. International Agency for Research on Cancer. IARC monographs on the evaluation of carcinogenic risks to humans. Air Pollution, Part 1. Some nonheterocyclic polycyclic aromatic hydrocarbons and some related industrial exposures, vol. 2010b; 92.World Health Organization, Lyon, France, http://monographs.iarc.fr/ENG/Meetings/92-pahs.pdf

  • Jarrett SG, Boulton ME (2005) Antioxidant up-regulation and increased nuclear DNA protection play key roles in adaptation to oxidative stress in epithelial cells. Free Radic Biol Med 38(10):1382–1391

    Article  CAS  Google Scholar 

  • Jeney V, Eaton JW, Balla G, Balla J (2013) Natural history of the bruise, formation, elimination and biological effects of oxidized hemoglobin. Oxidative medicine and cellular longevity article 2013; ID: 703571: 9. doi:10.1155/2013/703571

  • Jeng HA, Pan C-H, Linc W-Y, Wud M-T, Taylore S, Chang-Chienf G-P, Zhoug G, Diawarah N (2013) Biomonitoring of polycyclic aromatic hydrocarbons from coke oven emissions and reproductive toxicity in nonsmoking workers. J Hazard Mater 244–245:436–443

    Article  Google Scholar 

  • Jongeneelen FJ (2001) Benchmark guideline for urinary 1-hydroxypyrene as biomarker of occupational exposure to polycyclic aromatic hydrocarbons. Ann Occup Hyg 45:3–13

    Article  CAS  Google Scholar 

  • Jongeneelen FJ (2014) A guidance value of 1-hydroxypyrene in urine in view of acceptable occupational exposure to polycyclic aromatic hydrocarbons. Toxicol Lett 231(2):239–248

  • Jongeneelen FJ, Anzion RB, Leijdekkers CM, Bos RP, Henderson PT (1985) 1-hydroxypyrene in human urine after exposure to coal tar and a coal tar derived product. Int Arch Occup Environ Health 57:47–55

  • Kamal A, Malik RN, Martellini T, Cincinelli A (2014) PAHs exposure biomarkers are associated with clinico-chemical changes in the brick kiln workers in Pakistan. Sci Tot Environ 490:521–527

    Article  CAS  Google Scholar 

  • Kamal A, Cincinelli A, Martellini T, Malik RN (2015a) A review of PAH exposure from the combustion of biomass fuel and their less surveyed effect on the blood parameters. Environ Sci Pollut Res. doi:10.1007/s11356-014-3748-0

    Google Scholar 

  • Kamal A, Cincinelli A, Martellini T, Palchetti I, Bettazzi F, Malik RN (2015b) Health and carcinogenic risk evaluation for cohorts exposed to PAHs in petrochemical workplaces in Rawalpindi city (Pakistan). Int J Environ Health Res. doi:10.1080/09603123.2015.1007843

    Google Scholar 

  • Kato M, Loomis D, Brooks LM, Gattas GFJ, Gomes L, Carvalho AB (2004) Urinary biomarkers in charcoal workers exposed to wood smoke in Bahia State Brazil. Cancer Epidemiol Biomarkers Prev 13(6):1005–1012

    CAS  Google Scholar 

  • Kim H, Kim YD, Lee H, Kawamoto T, Yang M, Katoh T (1999) Assay of 2-naphthol in human urine by high-performance liquid chromatography. J Chromatogr B 734:211–217

    Article  CAS  Google Scholar 

  • Kim H, Hwang JY, Ha EH, Park H, Ha M, Lee SH, Hong YC, Chang N (2011) Fruit and vegetable intake influences the association between exposure to polycyclic aromatic hydrocarbons and a marker of oxidative stress in pregnant women. Eur J Clin Nutr 65:1118–1125

  • Kinnula VL, Crapo JD (2004) Superoxide dismutases in malignant cells and human tumors. Free Radic Biol Med 36:718–744

    Article  CAS  Google Scholar 

  • Knuckles ME, Inyang F, Ramesh A (2001) Acute and subchronic oral toxicities of benzo[a]pyrene in F-344 rats. Toxicol Sci 61:382–388

    Article  CAS  Google Scholar 

  • Kuusimaki L, Peltonen Y, Mutanen P, Peltonen K, Savela K (2004) Urinary hydroxy-metabolites of naphthalene, phenanthrene and pyrene as markers of exposure to diesel exhaust. Int Arch Occup Environ Health 77:23–30

    Article  Google Scholar 

  • Lal K, Mani U, Pandey R, Singh N, Singh A, Patel DK, Singh MP, Murth RC (2011) Multiple approaches to evaluate the toxicity of the biomass fuel cow dung (kanda)smoke Ecotoxicol. Environ Saf 74:2126–2132

    Article  CAS  Google Scholar 

  • Larson TV, Koenig JQ (1994) Wood smoke: emissions and non cancer respiratory effects. Annu Rev Public Health 15:133–156

    Article  CAS  Google Scholar 

  • Lauwerys RR (1997) Occupational toxicology. Cassett and Doull’s toxicology, fifthth edn. Pergamon Press, New York, Chapter 29

    Google Scholar 

  • Lee M-W, Chen M-L, Candice Lung S-C, Tsai C-J, Yin X-J, Mao I (2010) Exposure assessment of PM2.5 and urinary 8-OHdG for diesel exhaust emission inspector. Sci Tot Environ 408:505–510

    Article  CAS  Google Scholar 

  • Lee SF, Pervaiz S (2011) Assessment of oxidative stress-induced DNA damage by immunoflourescent analysis of 8-oxodG. Methods Cell Biol 103:99–113

    Article  CAS  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyragollol and a convenient assay for superoxide dismutase. Eur J Biochem 47(3):469–474

    Article  CAS  Google Scholar 

  • Martínez-Salinas RI, Leal ME, Batres-Esquivel LE, Domínguez-Cortinas G, Calderón J, Diaz-Barriga F, Pérez-Maldonado IN (2010) Exposure of children to polycyclic aromatic hydrocarbons in Mexico: assessment of multiple sources. Int Arch Occup Environ Health 83:617–623

    Article  Google Scholar 

  • Miah Md D, Rashid HA, Shin MY (2009) Wood fuel use in the traditional cooking stoves in the rural food plain areas of Bangladesh: a socio-environmental perspective. Biomass Bioenergy 33(1):70–78

    Article  Google Scholar 

  • Oh E, Im H, Kang HS, Jung W, Won NH, Lee E, Sul D (2006) Comparison of immunological and genotoxicological parameters in automobile emission inspectors exposed to polycyclic aromatic hydrocarbons. Environ Toxicol Pharmacol 21(1):108–117

    Article  CAS  Google Scholar 

  • Pavanello S, Kapka L, Siwinska E, Mielzy˜nska D, Bolognesi C, Clonfero E (2008) Micronuclei related to anti-B[a]PDE-DNA adduct in peripheral blood lymphocytes of heavily polycyclic aromatic hydrocarbon-exposed nonsmoking coke-oven workers and controls. Cancer Epidemiol. Biomark Prev 17:2795–2799

    Article  CAS  Google Scholar 

  • Pérez-Maldonado IN, Martínez-Salinas RI, Pruneda Alvarez LG, Pérez-Vázquez FJ (2014) Urinary 1-hydroxypyrene concentration from Mexican children living in the southeastern region in Mexico. Int J Environ Health Res 24(2):113–119. doi:10.1080/09603123.2013.800960

    Article  Google Scholar 

  • Pick WM, Ross MH, Dada Y (2002) The reproductive and occupational health of women street vendors in Johannesburg, South Africa. Soc Sci Med 54:193–204

    Article  Google Scholar 

  • Pope DP, Mishra V, Thompson L, Siddiqui AR, Rehfuess EA, Weber M, Bruce NG (2010) Risk of low birth weight and stillbirth associated with indoor air pollution from solid fuel use in developing countries. Epidemiol Rev 32(1):70–81

    Article  Google Scholar 

  • Prado GF, Zanetta DM, Arbex MA, Braga AL, Pereira LA, de Marchi MR, de Melo Loureiro AP, Marcourakis T, Sugauara LE, Gattás GJ, Gonçalves FT, Salge JM, Terra-Filho M, de Paula Santos U (2012) Burnt sugarcane harvesting: particulate matter exposure and the effects on lung function, oxidative stress, and urinary 1-hydroxypyrene. Sci Tot Environ 437:200–208

    Article  CAS  Google Scholar 

  • Preuss R, Koch HM, Wilhelm M, Pischetsrieder M, Angerer J (2004) Pilot study on the naphthalene exposure of German adults and children by means of urinary 1- and 2- naphthol levels. Int J Hyg Environ Health 207:441–445

    Article  CAS  Google Scholar 

  • Pruneda-Álvarez LG, Pérez-Vázquez FJ, Salgado-Bustamante M, Martínez-Salinas RI, Pelallo-Martínez NA, Pérez-Maldonado IN (2012) Exposure to indoor air pollutants (polycyclic aromatic hydrocarbons, toluene, benzene) in Mexican indigenous women. Indoor Air 22(2):140–147. doi:10.1111/j.1600-0668.2011.00750.x

    Article  Google Scholar 

  • Rajvanshi AK (2006) Ethanol fuel for rural households, Maharashtra, India: Nimbkar Agricultural Research Institute. http://nariphalatn.virtualave.net/ruralethanol.pdf Accessed 12 Dec 2009

  • Razavi SM, Nazifi S, Bateni M, Rakhshandehroo E (2011) Alterations of erythrocyte antioxidant mechanisms, antioxidant enzymes, lipid peroxidation and serum trace elements associated with anemia in bovine tropical theileriosis. Vet Parasitol 180(3–4):209–214

    Article  CAS  Google Scholar 

  • Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 49:1603–1616

    Article  CAS  Google Scholar 

  • Rihs H-P, Pesch B, Kappler M, Rabstein S, Robbach B, Angerer J, Scherenberg M, Adams A, Wilhelm M, Seidel A, Burning T (2005) Occupational exposure to polycyclic aromatic hydrocarbons in German industries Association between exogenous exposure and urinary metabolites and its modulation by enzyme polymorphisms. Toxicol Lett 157:241–255

    Article  CAS  Google Scholar 

  • Romieu I, Riojas-Rodriguez H, Marron-Mares AT, Schilmann A, Perez-Padilla R, Masera O (2009) Improved biomass stove intervention in rural Mexico, impact on the respiratory health of women. Am J Respir Crit Care Med 180(7):649–656

    Article  Google Scholar 

  • Ruíz-Vera T, Pruneda-Alvarez LG, Pérez-Vázquez FJ, Ochoa-Martínez AC, Orta-García ST, Ilizaliturri-Hernández CA, Pérez-Maldonado IN (2014) Using urinary 1-hydroxypyrene concentrations to evaluate polycyclic aromatic hydrocarbon exposure in women using biomass combustion as main energy source. Drug Chem Toxicol 13:1–6

    Google Scholar 

  • Sauvain A, Setyan JJ, Wild P, Tacchini P, Lagger G, Storti F, Deslarzes S, Guillemin M, Rossi MJ, Ridiker M (2011) Biomarkers of oxidative stress and its association with the urinary reducing capacity in bus maintenance workers. J Occup Med Toxico 6:18

    Article  Google Scholar 

  • Shealy DB, Barr JR, Ashley DL, Patterson DG Jr, Camann DE, Bond AE (1997) Correlation of environmental carbaryl measurements with serum and urinary 1-naphthol measurements in a farmer applicator and his family. Environ Health Perspect 105(5):510–513

    Article  CAS  Google Scholar 

  • Singh DP, Gadi R, Mandal TK, Saud T, Saxena M, Sharma SK (2013) Emissions estimates of PAH from biomass fuels used in rural sector of Indo-Gangetic Plains of India. Atmos Environ 68:120–126

    Article  CAS  Google Scholar 

  • Smith KR, Mehta S (2003) The burden of disease from indoor air pollution in developing countries: comparison of estimates. Int J Hyg Environ Health 206:279–289

    Article  CAS  Google Scholar 

  • Torres-Duque C, Maldonado D, Perez-Padilla R, Ezzatti M (2008) Biomass and fuels and respiratory diseases: a review of the evidence. Proc Am Thorac Soc 5(5):577–590

    Article  Google Scholar 

  • Trejo-Acevedo A, Rivero-Pérez NE, Flores-Ramírez R, Orta-García ST, Varela-Silva JA, Pérez-Maldonado IN (2012) Assessment of the levels of persistent organic pollutants and 1-hydroxypyrene in blood and urine samples from Mexican children living in an endemic malaria area in Mexico. Bull Environ Contam Toxicol 88(6):828–832. doi:10.1007/s00128-012-0593-z

    Article  CAS  Google Scholar 

  • Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552:335–344

    Article  CAS  Google Scholar 

  • UNDP/EW/WB. Household energy demand handbook for 1991: Pakistan household energy strategy study (HESS). Prepared by UNDP, Energy Wing and World Bank for the Government of Pakistan; 1993.

  • Unwin J, Cocker J, Scobbie E, Chambers H (2006) An assessment of occupational exposure to polycyclic aromatic hydrocarbons in the UK. Ann Occup Hyg 50:395–403

    Article  CAS  Google Scholar 

  • US. EPA, guidance on selecting age groups for monitoring and assessing childhood exposures to environ contam 2005; EPA/630/P-03/003F

  • Valavanidis A, Vlachogianni T, Fiotakis C (2009) 8-hydroxy-2′-deoxyguanosine (8-OHdG). a critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 27:120–139

    Article  CAS  Google Scholar 

  • Velema JP, Ferrera A, Figueroa M, Bulnes R, Toro LA, DE Barahona O, Claros JM, Melchers WJG (2002) Burning wood in the kitchen increases the risk of cervical neoplasia in HPV-infected women in Honduras. In J Cancer 97(4):536–541

    CAS  Google Scholar 

  • Wang J, Luo X, Xu B, Wei J, Zhang Z, Zhu H (2011) Elevated oxidative damage in kitchen workers in Chines restaurants. J Occup Health 53(5):327–333

    Article  CAS  Google Scholar 

  • WHO (2009) Global Health Risks: Mortality and burden of disease attributable to selected major risks. World Health Organization, Geneva. WHO. Situation analysis of household energy use and indoor air pollution in Pakistan. Discussion Paper on Child Health

  • WHSQ (2012) Workplace health and safety Queensland, Polycyclic aromatic hydrocarbons (PAH) health monitoring guidelines PN10470 Version 2. Last updated June 2012. www.worksafe.qld.gov.au

  • Wiegratz I, Kutschera E, Lee JH, Moore C, Mellinger U, Winkler UH, Kuhl H (2003) Effect of four oral contraceptives on thyroid hormones, adrenal and blood pressure parameters. Contraception 67(5):361–366

    Article  CAS  Google Scholar 

  • Wiegratz I, Lee JH, Kutschera E, Winkler UH, Kuhl H (2004) Effect of four oral contraceptives on hemostatic parameters. Contraception 70(2):97–106

    Article  CAS  Google Scholar 

  • Wilhelm M, Hardt J, Schulz C, Angerer J (2008) New reference value and the background exposure for the PAH metabolites 1-hydroxypyrene and 1- and 2-naphthol in urine of the general population in Germany: basis for validation of human biomonitoring data in environmental medicine. Int J Hyg Environ Health 211(3–4):447–453

    Article  CAS  Google Scholar 

  • Winterbourn CC, Hawkins RE, Brian M, Carrell RW (1975) The estimation of red cell superoxide dismutase activity. J Lab Clin 85(2):337–341

    CAS  Google Scholar 

  • Wood-Kaczmar A, Gandhi S, Wood NW (2006) Understanding the molecular causes of Parkinson’s disease. Trends Mol Med 12(11):521–528

  • Xu X, Zhang J, Zhang L, Liu W, Weisel CP (2004) Selective detection of monohydroxy metabolites of polycyclic aromatic hydrocarbons in urine using liquid chromatography/ triple quadrupole tandem mass spectrometry. Rapid Commun Mass Spectrom 18(19):2299–2308

    Article  CAS  Google Scholar 

  • Yoon H-S, Lee K-M, Lee K-H, Kim S, Choid K, Daehe K (2013) Polycyclic aromatic hydrocarbon (1-OHPG and 2-naphthol) and oxidative stress (malondialdehyde) biomarkers in urine among Korean adults and children. Int J Hyg Environ Health 215:458–464

    Article  Google Scholar 

  • Zelikoff JT, Chen LC, Cohen MD, Schlesinger RB (2002) The toxicology of inhaled wood smoke. J Toxicol Environ Health 5(3):269–282

    Article  CAS  Google Scholar 

  • Zhang JJ, Smith KR (2007) Household air pollution from coal and biomass fuels in China: measurements, health impacts, and interventions. Environ Health Perspect 115(6):848–855

    Article  Google Scholar 

  • Zhang JJ, Smith KR (2003) Indoor air pollution: a global health concern. Br Med Bull 68(1):209–225. doi:10.1093/bmb/ldg029

    Article  CAS  Google Scholar 

  • Zhang Y, Ding J, Shen G, Zhong J, Wang C, Wei S, Chen C, Chen Y, Lu Y, Shen H, Li W, Huang Y, Chen H, Su S, Lin N, Wang X, Liu W, Tao S (2014) Dietary and inhalation exposure to polycyclic aromatic hydrocarbons and urinary excretion of monohydroxy metabolites — a controlled case study in Beijing, China. Environ Pollut 184:515–522

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Acknowledgments

This work was supported by the Department of Chemistry “Ugo Schiff”, University of Florence, Italy. We acknowledge the Higher-Education Commission, Pakistan (HEC) for providing financial support for the research work under the International Research Support Initiative Program (IRSIP).

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Kamal, A., Cincinelli, A., Martellini, T. et al. Biomarkers of PAH exposure and hematologic effects in subjects exposed to combustion emission during residential (and professional) cooking practices in Pakistan. Environ Sci Pollut Res 23, 1284–1299 (2016). https://doi.org/10.1007/s11356-015-5297-6

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