Comparing the metal concentration in the hair of cancer patients and healthy people living in the Malwa region of Punjab, India

Clinical Medicine Insights: Oncology

Volumn 8, Issue , 2014, Pages 1-13

  Blaurock Busch, Eleonore ^a,b   Busch, Yvette M ^b   Friedle, Albrecht ^c   Buerner, Holger ^a,b   Parkash, Chander ^d   Kaur, Anudeep ^d  

^a Trace Minerals International   (United States)

^b Micro Trace Minerals ^*  (Germany)

^c Labor Friedle GmbH   (Germany)

^d I K GUJRAL PUNJAB TECHNICAL UNIVERSITY   (India)

Author keywords

Barium; Breast cancer; Cancer; Hair analysis; Lead; Malwa region; Punjab; Strontium; Uranium

Indexed keywords

ALUMINUM; BARIUM; DRINKING WATER; LEAD; MANGANESE; METAL; PHOSPHATE FERTILIZER; STRONTIUM; URANIUM;

ADULT; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER PATIENT; CLINICAL ARTICLE; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; HAIR LEVEL; HUMAN; INDIA; LONG TERM EXPOSURE; MALE; OCCUPATIONAL EXPOSURE; PREVALENCE; SOIL POLLUTION; WATER CONTAMINATION;

EID: 84892180073     PISSN: 11795549     EISSN: 11795549     Source Type: Journal    
DOI: 10.4137/CMO.S13410     Document Type: Article

References (120)

1. Dept of Health and Family Welfare. State Wide Door to Door Campaign, Cancer Awareness and Symptom Based Early Detection. Government of Punjab, Chandigarh, India. 2013.
2. Singh BP. Cancer deaths in agricultural heartland: a study in Malwa region of Indian Punjab. [Master thesis]. Enschede: International Institute for Geo-Information Science and Earth Observation (ITC), University of Twente; 2008.
3. Mittal S, Kaur G, Vishwakarma GS. Effects of environmental pesticides on the health of rural communities in the Malwa region of Punjab (India): a review. Human and Ecological Risk Assessment: An International Journal. 2013, in press.
4. Koutros S, Alavanja MC, Lubin JH, et al. An update of cancer incidence in the Agricultural Health Study. J Occup Environ Med. 2010;52:1098-105.
5. Ilychova SA, Zaridze DG. Cancer mortality among female and male workers occupationally exposed to inorganic lead in the printing industry. Occup Environ Med. 2012;69:87-92.
6. Qu W, Tokar EJ, Kim AJ, Bell MW, Waalkes MP. Chronic cadmium exposure in vitro causes acquisition of multiple tumor cell characteristics in human pancreatic epithelial cells. Environ Health Perspect. 2012;120:1265-71.
7. Cheung MR. Blood lead concentration correlates with all cause, all cancer and lung cancer mortality in adults: a population based study. Asian Pac J Cancer Prev. 2013;14:3105-8.
8. Person RJ, Tokar EJ, Xu Y, Orihuela R, Ngalame NN, Waalkes MP. Chronic cadmium exposure in vitro induces cancer cell characteristics in human lung cells. Toxicol Appl Pharmacol. In press.
9. Stoica A, Katzenellenbogen BS, Martin MB. Activation of estrogen receptor-alpha by the heavy metal cadmium. Mol Endocrinol. 2000;14:545-53.
10. Stohs SJ, Bagchi D. Mechanisms in the Toxicity of Metal Ions. Free Radical Biology and Med. 1995;18(2):321-36.
11. Türkdoǧan MK, Kilicel F, Kara K, Tuncer I, Uygan I. Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environ Toxicol Pharmacol. 2003;13:175-9.
12. Koivistoinen P, ed. Mineral Element Composition of Finnish Foods: N, K, Ca, Mg, P, S, Fe, Cu, Mn, Zn, Mo, Co, Ni, Cr, F, Se, Si, Rb, Al, B, Br, Hg, As, Cd, Pb, and Ash. In: Acta Agriculturae Scandinavica, Supplementum 22. Stockholm: Scandinavian Association of Agricultural Scientists and the Royal Swedish Academy of Agriculture and Forestry; 1980.
13. Sharma R. Analysis of water quality parameters of groundwater in Malwa region, Bathinda, India. Asian J of Adv Scientific and Engineering Res. 2012;1(11). http://ajaser.com/rajnisharma.pdf.
14. Aulakh MS, Mohinder PS, Khurana MPS, Singh D. Water pollution related to agricultural, industrial, and urban activities, and its effects on the food chain: Case studies from Punjab. Journal of New Seeds. 2009;10:112-37.
15. Sabha R. Uranium in Ground Water. Gov. of India, Dept. Atomic Energy Statement. August 30, 2012.
16. World Health Organization. Uranium in drinking-water. Background document for development of WHO Guidelines for Drinking-water Quality. Geneva: World Health Organization; 2011. http://www.who.int/water_sanitation_health/dwq/chemicals/uranium_forcomment_20110211_en.pdf. Accessed Oct 2012.
17. Umweltbundesamt. Uran (U) im Trinkwasser: Kurzbegründung des gesundheitlichen Grenzwertes der Trinkwasserversorgung (10 mikro g/l U) und des Grenzwertes für "säuglingsgeeignete" abgepackte Wässer (2 mikro g/l U). Dessau-Roßlau: Umweltbundesamt; 2013. http://www.umweltdaten.de/publikationen/fpdf-l/4193.pdf.
18. Kumar A, Rout S, Narayanan U, et al. Geochemical modeling of uranium specification in the subsurface aquatic environment of Punjab State in India. J of Geo Min Res. 2011;3(5):137-46.
19. Szynkowska MI, Pawlaczyk A, Wojciechowska E, Sypniewski S, Paryjczak T. Human hair as a biomarker in assessing exposure to toxic metals. Pol J Environ Stud. 2009;18:1151-61.
20. Thomas L. Labor und Diagnose. Med. Verlag Marburg. 1992;(4):430.
21. Meißner D, Klemm M, Zogbaum M. Problematik, Klinik und Beispiele der Spurenelementvergiftung-Blei. Toxicchem Krimtech. 2011;78(3):453-63.
22. Hac E, Krechniak J. Lead levels in bone and hair of rats treated with lead acetate. J Biol Trace Element Res. 1996;52:293.
23. Mestek O, Deyl Z, Miksik I, Nowotna J, Pfeifer I, Herget J. Accumulation of lead in tissues after its administration in drinking water to laboratory rats. Physiol Res.1998;47:197-202.
24. Wilhelm M, Idel H. Hair analysis in environmental medicine. Zbl Hyg. 1996;198:485-501.
25. Environmental Protection Agency. Uranium. Radiation Protection. 2012. http://www.epa.gov/radiation/radionuclides/uranium.html. Accessed Oct 2012.
26. Pinney SM, Yaghjyan L, Buckholz JM, et al. Breast cancer incidence is related to uranium particulate exposure in a population living near a uranium refinery. Dept Environ Health, University of Cincinnati. Publ in progress.
27. Horn PS, Pesce AJ. Reference intervals: an update. Clin Chim Acta. 2003; 334:5-23.
28. Schlatter C. Environmental pollution and human health. Sci Total Environ. 1994;143:93-101.
29. Järup L. Hazards of heavy metal contamination. Br Med Bull. 2003;68:167-82.
30. Skerfving S, Nilsson U. Assessment of accumulated body burden of metals. Toxicol Lett. 1992;64/65:17-24.
31. Batzevich VA. Hair trace element analysis in human ecology studies. Sci Total Environ. 1995;164:89-98.
32. Ionescu JG, Novotny J, Stejskal V, Lätsch A, Blaurock-Busch E, Eisenmann-Klein M. Increased levels of transition metals in breast cancer tissue. Neuro Endocrinol Lett. 2006;27(Suppl 1):36-9.
33. Chiou HY, Hsueh YM, Liaw K-F, et al. Incidence of Internal Cancers and Ingested Inorganic Arsenic: A Seven-Year Follow-up Study in Taiwan. Cancer Res. 1995;55:1296.
34. Chen Y, Ahsan H. Cancer Burden From Arsenic in Drinking Water in Bangladesh. American J Public Health. 2004;94(5):741-4.
35. Smith AH, Hopenhayn-Rich C, Bates MN, et al. Cancer risks from arsenic in drinking water. Environ Health Perspect. 1992;97:259-67.
36. Antila E, Mussalo-Rauhamaa H, Kantola M, Atrishi F, Westermarck T. Association of cadmium with human breast cancer. Sci Total Environm. 1996;186(3):251-6
37. Åkesson A, Julin B, Wolk A. Long-term Dietary Cadmium Intake and Postmenopausal Endometrial Cancer Incidence: A Population-Based Prospective Cohort Study. Cancer Res. 2008;68(15):6435-41.
38. Garcia-Morales P, Saceda M, Kenney N, et al. Effect of cadmium on estrogen receptor levels and estrogen-induced responses in human breast cancer cells. J Biol Chem. 1994;269(24):16896-901.
39. Darbre PD. Aluminium, antiperspirants and breast cancer. J Inorg Biochem. 2005;99(9):1912-9.
40. Mannello F, Ligi D, Canale M. Aluminium, carbonyls and cytokines in human nipple aspirate fluids: Possible relationship between inflammation, oxidative stress and breast cancer microenvironment. J Inorg Biochem. 2013;128:250-6.
41. Mannello F, Tonti GA, Medda V, Simone P, Darbre PD. Analysis of aluminium content and iron homeostasis in nipple aspirate fluids from healthy women and breast cancer-affected patients. J Appl Toxicol. 2011;31(3):262-9.
42. Sekhon GS, Singh B. Estimation of Heavy Metals in the Groundwater of Patiala District of Punjab, India. Earth Resources. 2013;1(1):1-4.
43. Tripathi RM, Mahapatra S, Raghunath R, Vinod Kumar A, Sadasivan S. Daily intake of aluminium by adult population of Mumbai, India. Sci Total Environ. 2002;299:73-7.
44. Gramiccioni L, Ingrao G, Milana MR, Santaroni P, Tomassi G. Aluminium levels in Italian diets and in selected foods from aluminium utensils. Food Addit Contam. 1996;13(7):767-74.
45. Corbillon MS, Olazabal MA, Madariaga JM. Potentiometric study of aluminium-fluoride complexation equilibria and definition of the thermodynamic model. J Solution Chem. 2008;37:567-79.
46. Greger JL. Dietary and other sources of aluminium intake. Ciba Found Symp. 1992;169:26-35; discussion 35-49.
47. Agency for Toxic Substances and Disease Registry (2007). Toxicological profile for barium. US Department of Health and Human Services. Atlanta, GA: Public Health Service, 2007.
48. Wise SS, Holmes AL, Qin Q, et al. Comparative Genotoxicity and Cytotoxicity of Four Haxevalent Chromium Compounds in Human Bronchial Cells. Chem. Res. Toxicol. 2010;23,365-72.
49. EEC (1976) Council Directive 76/768/EC of 27 July on the approximation of the laws of Member States relating to cosmetic products. Official Journal of European Communities 1976; No. L262: 169-200. This directive was replaced by Regulation (EC) No 1223/2009 from 11 July 2013.
50. Dallas CE, Williams PL. Barium: rationale for a new oral reference dose. J Toxicol Environ Health B Crit Rev. 2001;4:395-429.
51. Parekh PP, Khan AR, Torres MA, Kitto ME. Concentrations of selenium, barium, and radium in Brazil nuts. J Food Comp Anal. 2008;21:332-5.
52. Underwood E. Trace Elements in Human Health and Disease. 4th Ed. New York: Academic Press, 1977.
53. Hurley L, Keen C. Manganese. In: Mertz W. (Ed). Trace Elements in Human and Animal Nutrition. 5th ed. Vol. 1. San Diego: Academic Press, 1987;185-224.
54. ATSDR (2012). Toxicological profile for manganese. US Department of Health and Human Services. Atlanta, GA: Public Health Service, 2012.
55. Gerber GB, Léonard A, Hantson P. Carcinogenicity, mutagenicity and teratogenicity of manganese compounds. Crit Rev Oncol Hematol. 2002;42(1):25-34.
56. Floriańczyk B, Grzybowska L, Marzec Z. Metallothionein and manganese concentrations in breast cancer and mastopathic tissues. J Pre-Clin and Clin Res. 2011;5(2):63-5.
57. Krauskopf KB. Separation of manganese from iron in sedimentary processes. Geochim. Cosmochim. Acta. 1957;12:61-84.
58. Schulte EE, Kelling KA. Soil and Applied Manganese. UW Extension. 2004; A2526.
59. Christophersen OA. Some aspects of the biogeochemical behavior of manganese as compared to other elements. In: Låg J (Ed.). Geomedical problems related to aluminium, iron and manganese. Oslo: Det Norske Videnskaps-Akademi; 1994, p.85-99.
60. Blume H-P, Brümmer GW, Horn R, et al. Scheffer/Schachtschabel: Lehrbuch der Bodenkunde. 16. Aufl., XIV, 570 S. Springer-Spektrum, 2010.
61. Marschner P (Ed.). Marschner's Mineral Nutrition of Higher Plants (Third Edition). Academic Press, CA Elsevier 2012.
62. Wallis JA. Intensified systems of farming in the tropics and subtropics. World Bank discussion papers 364. Washington, DC: World Bank, 1997.
63. St Clair DK, Holland JC. Complementary DNA encoding human colon cancer manganese superoxide dismutase and the expression of its gene in human cells. Cancer Res. 1991;51:939-43.
64. Sun GG, Wang YD, Yu XR, et al. Expression of MnSOD mRNA and protein in esophageal squamous cell carcinoma and its clinical significance (in Chinese). Zhonghua Zhong Liu Za Zhi. 2010;32:834-7.
65. Zhou J, Du Y. Acquisition of resistance of pancreatic cancer cells to 2-methoxyestradiol is associated with the upregulation of manganese superoxide dismutase. Mol Cancer Res. 2012;10:768-77.
66. Li JJ, Oberley LW, St Clair DK, Ridnour LA, Oberley TD. Phenotypic changes induced in human breast cancer cells by overexpression of manganese-containing superoxide dismutase. Oncogene. 1995;10:1989-2000.
67. Spangler JG, Reid JC. Environmental manganese and cancer mortality rates by county in North Carolina: an ecological study. Biol Trace Elem Res. 2010;133:128-35.
68. Sachdev HP, Gera T. Preventing childhood anemia in India: iron supplementation and beyond. Eur J Clin Nutr. 2013;67:475-80.
69. Swaminathan S, Edward BS, Kurpad AV. Micronutrient deficiency and cognitive and physical performance in Indian children. Eur J Clin Nutr. 2013;67:467-74.
70. Thankachan P, Selvam S, Surendran D, et al. Efficacy of a multi micronutrient-fortified drink in improving iron and micronutrient status among schoolchildren with low iron stores in India: a randomised, double-masked placebo-controlled trial. Eur J Clin Nutr. 2013;67:36-41.
71. Bharti S, Bharti B, Naseem S, Attri SV. A community-based cluster randomized controlled trial of "directly observed home-based daily iron therapy" in lowering prevalence of anemia in rural women and adolescent girls. Asia Pac J Public Health. In press.
72. Muthayya S, Rah JH, Sugimoto JD, Roos FF, Kraemer K, Black RE. The global hidden hunger indices and maps: an advocacy tool for action. PLoS One. In press.
73. Christophersen OA. Radiation biochemistry. In: Brune D, Hellborg R, Persson BRR, Pääkkönen R (Eds.). Radiation at Home, Outdoors and in the Workplace. Oslo, Norway: Scandinavian Science Publishers; 2001:52-61.
74. García-Lestón J, Roma-Torres J, Vilares M, et al. Genotoxic effects of occupational exposure to lead and influence of polymorphisms in genes involved in lead toxicokinetics and in DNA repair. Environ Int. 2012;43:29-36.
75. Kašuba V, Rozgaj R, Milić M, et al. Evaluation of genotoxic effects of lead in pottery-glaze workers using micronucleus assay, alkaline comet assay and DNA diffusion assay. Int Arch Occup Environ Health. 2012;85:807-18.
76. Yang JL, Wang LC, Chang CY, Liu TY. Singlet oxygen is the major species participating in the induction of DNA strand breakage and 8-hydroxydeoxyguanosine adduct by lead acetate. Environ Mol Mutagen. 1999;33:194-201.
77. Steenland K, Boffetta P. Lead and Cancer in Humans: Where Are We Now? Am J Ind Med. 2000;38:295-9.
78. Menezes-Filho JA, Viana GF, Paes CR. Determinants of lead exposure in children on the outskirts of Salvador, Brazil. Environ Monit Assess. 2012;184 2593-603.
79. Cadwalader GO, Renshaw CE, Jackson BP, Magilligan FJ, Landis JD, Bostick BC. Erosion and physical transport via overland flow of arsenic and lead bound to silt-sized particles. Geomorphology (Amst). 2011;128:85-91.
80. Delistraty D, Yokel J. Ecotoxicological study of arsenic and lead contaminated soils in former orchards at the Hanford site, USA. Environ Toxicol. In press.
81. Dheri GS, Brar MS, Malhi SS. Heavy-metal concentration of sewage-contaminated water and its impact on underground water, soil and crop plants in alluvial soils of Northwestern India. Comm Soil Sci Plant Analysis. 2007;38:1353-70.
82. Kaur S. Lead in the scales of cobras and wall lizards from rural and urban areas of Punjab, India. Sci Total Environ. 1988;77:289-90.
83. Flora G, Gupta D, Tiwari A. Toxicity of lead: A review with recent updates. Interdiscip Toxicol. 2012;5:47-58.
84. Kennedy DA, Woodland C, Koren G. Lead exposure, gestational hypertension and pre-eclampsia: a systematic review of cause and effect. J Obstet Gynaecol. 2012;32:512-7.
85. Petrović V, Colović M, Krstić D, et al. In vitro effects of some gold complexes on Na+/K+ ATPase activity and cell proliferation. J Inorg Biochem. 2013;124:35-41.
86. Yuan Y, Jiang CY, Xu H, et al. Cadmium-induced apoptosis in primary rat cerebral cortical neurons culture is mediated by a calcium signaling pathway. PLoS One. 2013;8:e64330.
87. Zaidi A. Plasma membrane Ca-ATPases: Targets of oxidative stress in brain aging and neurodegeneration. World J Biol Chem. 2010;1:271-80.
88. Hettiarachchi NT, Boyle JP, Bauer CC, et al. Peroxynitrite mediates disruption of Ca2+ homeostasis by carbon monoxide via Ca2+ ATPase degradation. Antioxid Redox Signal. 2012;17:744-55.
89. Sandhir R, Gill KD. Alterations in calcium homeostasis on lead exposure in rat synaptosomes. Mol Cell Biochem. 1994;131:25-33.
90. Baranowska-Bosiacka I, Gutowska I, et al. Altered energy status of primary cerebellar granule neuronal cultures from rats exposed to lead in the pre-and neonatal period. Toxicology. 2011;280:24-32.
91. MacDonald E, Hellevuo K, Komulainen H. Lead does not affect calmodulin-induced activation of calcium-dependent adenosine triphosphatase in human red blood cell membranes. Arch Toxicol Suppl. 1986;9:397-400.
92. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Inorganic and organic lead compounds. IARC Monogr Eval Carcinog Risks Hum. 2006;87:1-471.
93. Garmash SA, Smirnova VS, Karp OE, et al. Pro-oxidative, genotoxic and cytotoxic properties of uranyl ions. J Environ Radioact. In press.
94. Krauskopf KB, Bird DK. Introduction to Geochemistry. McGraw Hill. 1995;3:647.
95. Mehta D. Uranium in Ground Water Region. Private communication. Scientific opinion and fact sheet 2005. http://physics.puchd.ac.in./dmetha/uranium-facts.doc.
96. Marie PJ, Ammann P, Boivin G, Rey C. Mechanisms of action and therapeutic potential of strontium in bone. Calcif Tissue Int. 2001;69:121-9.
97. Omdahl JL, DeLuca HF. Rachitogenic activity of dietary strontium. I. Inhibition of intestinal calcium absorption and 1,25-dihydroxycholecalciferol synthesis. J Biol Chem. 1972;247:5520-6.
98. EPA. 2012 Edition of the Drinking Water Standards and Health Advisories. EPA 822-S-12-001. Washington, DC: Office of Water, U.S. Environmental Protection Agency, 2012.
99. Blaurock-Busch E, Friedle A, Godfrey M, Schulte-Uebbing CE, Smit C. Metal exposure in the children of Punjab, India. Clinical Medicine Insights: Therapeutics. 2010;2:655-61.
100. Mehra R, Singh S, Singh K. Uranium studies in water samples belonging to Malwa Region of Punjab, using track etching technique. Radiat Meas. 2007;42:441-5.
101. Mehra R, Singh S, Singh K. A study of uranium, radium, radon exhalation rate and indoor radon in the environs of some areas of the Malwa region, Punjab. Indoor Built Environ. 2006;15:499-505.
102. Garrels R, Christ CL. Solutions, Minerals, and Equilibria. Harpers' Geoscience Series. New York: Harper and Row, 1965.
103. Khater AE. Uranium and trace elements in phosphate fertilizers-Saudi Arabia. Health Phys. 2012;102:63-70.
104. Singh J, Dhaliwal TK, Grover DK. State Agricultural Profile-Punjab. AERC Study No. 30. Ludhiana: Agro-Economic Research Centre, Department of Economics and Sociology, Punjab Agricutural University, 2012.
105. Homma-Takeda S, Kokubo T, Terada Y, et al. Uranium dynamics and developmental sensitivity in rat kidney. J Appl Toxicol. 2013;33:685-94.
106. Kurttio P, Auvinen A, Salonen L, et al. Renal Effects of Uranium in Drinking Water. Environm Health Perspectives. 2002;110(4):337-42.
107. Allodji RS, Leuraud K, Thiébaut AC, Henry S, Laurier D, Bénichou J. Impact of measurement error in radon exposure on the estimated excess relative risk of lung cancer death in a simulated study based on the French Uranium Miners' Cohort. Radiat Environ Biophys. 2012;51:151-63.
108. Heidenreich WF, Tomasek L, Grosche B, Leuraud K, Laurier D. Lung cancer mortality in the European uranium miners cohorts analyzed with a biologically based model taking into account radon measurement error. Radiat Environ Biophys. 2012;51:263-75.
109. Rage E, Vacquier B, Blanchardon E, et al. Risk of lung cancer mortality in relation to lung doses among French uranium miners: follow-up 1956-1999. Radiat Res. 2012;177:288-97.
110. Tirmarche M, Harrison J, Laurier D, Blanchardon E, Paquet F, Marsh J. Risk of lung cancer from radon exposure: contribution of recently published studies of uranium miners. Ann ICRP. 2012;41:368-77.
111. Tomasek L. Lung cancer mortality among Czech uranium miners-60 years since exposure. J Radiol Prot. 2012;32:301-14.
112. Hunter N, Muirhead CR, Tomasek L, et al. Joint analysis of three European nested case-control studies of lung cancer among radon exposed miners: exposure restricted to below 300 WLM. Health Phys. 2013;104:282-92.
113. Samet JM, Kutvirt DM, Waxweiler RJ, Key CR. Uranium mining and lung cancer in Navajo men. N Engl J Med. 1984;310:1481-4.
114. Al-Dujaily EA, Al-Janabi AA, Pierscionek T, Yasseen AA. High prevalence of HER-2/neu overexpression in female breast cancer among an Iraqi population exposed to depleted uranium. J Carcinog. 2008;7:8.
115. Raymond-Whish S, Mayer LP, O'Neal T, et al. Drinking water with uranium below the US EPA water standard causes estrogen receptor-dependent responses in female mice. Environ Health Perspect. 2007;115:1711-6.
116. Pratviel G. Oxidative DNA damage mediated by transition metal ions and their complexes. Met Ions Life Sci. 2012;10:201-16.
117. Hu J, Mao Y, White K. The Canadian Cancer Registries Epidemiology Research Group. Renal cell carcinoma and occupational exposure to chemicals in Canada. Occup Med. 2002;52:157-64.
118. Hayes RB. The carcinogenicity of metals in humans. Cancer Causes and Control. 1997;8:371-85.
119. Arruda VR, Grignoli CF, Goncalves MS, et al. Prevalence of homozygosity for the deleted alleles of glutathione S-transferase mu (GSTM1) and theta (GSTT1) among distinct ethnic groups from Brazil: relevance to environmental carcinogenesis? Clinical Genetics. 1998;54(3):210-4.
120. Harrison DJ. Frequency of glutathione S-transferase M1 deletion in smokers with emphysema and lung cancer. Hum Exp Toxicol. 1997;16(79):356-60.