Toxic impact of bromide and iodide on drinking water disinfected with chlorine or chloramines

Environmental Science and Technology

Volumn 48, Issue 20, 2014, Pages 12362-12369

  Yang, Yang ^a   Komaki, Yukako ^b,c   Kimura, Susana Y ^b,c   Hu, Hong Ying ^a   Wagner, Elizabeth D ^c   Mariñas, Benito J ^b,c   Plewa, Michael J ^c  

^a TSINGHUA UNIVERSITY   (China)

^b University of Illinois at Urbana Champaign   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROMIDE; CHLORINE; DRINKING WATER; GENOMIC DNA; IODIDE; MONOCHLORAMINE; CHLORAMINE DERIVATIVE; DISINFECTANT AGENT; TOSYLCHLORAMIDE SODIUM;

AMMONIA; BROMIDE; CHLORINE; DISINFECTION; DRINKING WATER; GENOTOXICITY; IODIDE; ORGANIC MATTER; TOXICITY;

ANIMAL TISSUE; ARTICLE; BROMINATION; CHLORINATION; CHO CELL LINE; CONCENTRATION RESPONSE; CORRELATION ANALYSIS; CYTOTOXICITY; DISINFECTION; DNA DAMAGE; FEMALE; GENOTOXICITY; IODINATION; MAMMAL CELL; NONHUMAN; ANIMAL; CHEMISTRY; COMPARATIVE STUDY; CRICETULUS; HALOGENATION; TOXICITY TESTING; WATER MANAGEMENT;

ANIMALS; BROMIDES; CHLORAMINES; CHLORINE; CHO CELLS; CRICETULUS; DISINFECTANTS; DISINFECTION; DRINKING WATER; HALOGENATION; IODIDES; TOXICITY TESTS; WATER PURIFICATION;

EID: 84908138349     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es503621e     Document Type: Article

References (85)

1. Akin, E. W.; Hoff, J. C.; Lippy, E. C. Waterborne outbreak control: Which disinfectant? Environ. Health Perspect. 1982, 46, 7-12
2. Richardson, S. D.; Postigo, C., Drinking water disinfection by-products. In Emerging Organic Contaminants and Human Health; Springer: Berlin, Germany, 2012; pp 93-137.
3. Singer, P. C. Control of disinfection by-products in drinking water J. Environ. Eng. 1994, 120 (4) 727-744
4. Hong, H.; Xiong, Y.; Ruan, M.; Liao, F.; Lin, H.; Liang, Y. Factors affecting THMs, HAAs and HNMs formation of Jin Lan Reservoir water exposed to chlorine and monochloramine Sci. Total Environ. 2013, 444, 196-204
5. Zhang, X.; Echigo, S.; Minear, R. A.; Plewa, M. J., Characterization and comparison of disinfection by-products of four major disinfectants. In Natural Organic Matter and Disinfection By-Products: Characterization and Control in Drinking Water; Barrett, S. E.; Krasner, S. W.; Amy, G. L., Eds.; American Chemical Society: Washington, D.C., 2000; pp 299-314.
6. Hua, G. H.; Reckhow, D. A. Comparison of disinfection byproduct formation from chlorine and alternative disinfectants Water Res. 2007, 41 (8) 1667-1678
7. Rook, J. J. Formation of haloforms during chlorination of natural waters Water Treat. Exam. 1974, 23, 234-243
8. Bellar, T. A.; Lichtenbert, J. J.; Kroner, R. C. The occurrence of organohalides in chlorinated drinking waters J. Am.Water Works Assoc. 1974, 66 (12) 703-706
9. Richardson, S. D., Disinfection by-products: Formation and occurrence in drinking water. In Encyclopedia of Environmental Health; Nriagu, J. O., Ed.; Elsevier: Burlington, 2011; Vol. 1, pp 110-136.
10. Richardson, S. D.; Plewa, M. J.; Wagner, E. D.; Schoeny, R.; DeMarini, D. M. Occurrence, genotoxicity, and carcinogenicity of regulated and emerging disinfection by-products in drinking water: A review and roadmap for research Mutat. Res. 2007, 636, 178-242
11. Plewa, M. J.; Wagner, E. D., Drinking water disinfection by-products: Comparative mammalian cell cytotoxicity and genotoxicity. In Encyclopedia of Environmental Health; Nriagu, J. O., Ed.; Elsevier: Burlington, 2011; Vol. 1, pp 806-812.
12. Plewa, M. J.; Wagner, E. D. Mammalian Cell Cytotoxicity and Genotoxicity of Disinfection By-Products; Water Research Foundation: Denver, CO, 2009; p 134.
13. Nieuwenhuijsen, M. J.; Grellier, J.; Smith, R.; Iszatt, N.; Bennett, J.; Best, N.; Toledano, M. The epidemiology and possible mechanisms of disinfection by-products in drinking water Philos. Trans. R. Soc., A 2009, 367 (1904) 4043-4076
14. Costet, N.; Villanueva, C. M.; Jaakkola, J. J.; Kogevinas, M.; Cantor, K. P.; King, W. D.; Lynch, C. F.; Nieuwenhuijsen, M. J.; Cordier, S. Water disinfection by-products and bladder cancer: Is there a European specificity? A pooled and meta-analysis of European case-control studies Occup. Environ. Med. 2011, 68 (5) 379-385
15. Villanueva, C. M.; Cantor, K. P.; Cordier, S.; Jaakkola, J. J.; King, W. D.; Lynch, C. F.; Porru, S.; Kogevinas, M. Disinfection byproducts and bladder cancer: A pooled analysis Epidemiology 2004, 15 (3) 357-367
16. Bove, G. E.; Rogerson, P. A.; Vena, J. E. Case-control study of the effects of trihalomethanes on urinary bladder cancer risk Arch. Environ. Occup. Health 2007, 62 (1) 39-47
17. King, W. D.; Marrett, L. D.; Woolcott, C. G. Case-control study of colon and rectal cancers and chlorination by-products in treated water Cancer Epidemiol. Biomarkers Prev. 2000, 9 (8) 813-818
18. Rahman, M. B.; Driscoll, T.; Cowie, C.; Armstrong, B. K. Disinfection by-products in drinking water and colorectal cancer: A meta-analysis Int. J. Epidemiol. 2010, 39 (3) 733-745
19. Bove, G. E., Jr.; Rogerson, P. A.; Vena, J. E. Case control study of the geographic variability of exposure to disinfectant byproducts and risk for rectal cancer Int. J. Health. Geogr. 2007, 6, 18
20. Waller, K.; Swan, S. H.; Windham, G. C.; Fenster, L. Influence of exposure assessment methods on risk estimates in an epidemiologic study of total trihalomethane exposure and spontaneous abortion J. Exposure Anal. Environ. Epidemiol. 2001, 11 (6) 522-531
21. Swan, S. H.; Waller, K.; Hopkins, B.; Windham, G.; Fenster, L.; Schaefer, C.; Neutra, R. R. A prospective study of spontaneous abortion: Relation to amount and source of drinking water consumed in early pregnancy Epidemiology 1998, 9 (2) 126-133
22. Hoffman, C. S.; Mendola, P.; Savitz, D. A.; Herring, A. H.; Loomis, D.; Hartmann, K. E.; Singer, P. C.; Weinberg, H. S.; Olshan, A. F. Drinking water disinfection by-product exposure and fetal growth Epidemiology 2008, 19 (5) 729-737
23. Righi, E.; Bechtold, P.; Tortorici, D.; Lauriola, P.; Calzolari, E.; Astolfi, G.; Nieuwenhuijsen, M. J.; Fantuzzi, G.; Aggazzotti, G. Trihalomethanes, chlorite, chlorate in drinking water and risk of congenital anomalies: A population-based case-control study in Northern Italy Environ. Res. 2012, 116, 66-73
24. Costet, N.; Garlantezec, R.; Monfort, C.; Rouget, F.; Gagniere, B.; Chevrier, C.; Cordier, S. Environmental and urinary markers of prenatal exposure to drinking water disinfection by-products, fetal growth, and duration of gestation in the PELAGIE birth cohort (Brittany, France, 2002-2006) Am. J. Epidemiol. 2012, 175 (4) 263-275
25. Jeong, C. H.; Wagner, E. D.; Siebert, V. R.; Anduri, S.; Richardson, S. D.; Daiber, E. J.; McKague, A. B.; Kogevinas, M.; Villanueva, C. M.; Goslan, E. H.; Luo, W.; Isabelle, L. M.; Pankow, J. F.; Grazuleviciene, R.; Cordier, S.; Edwards, S. C.; Righi, E.; Nieuwenhuijsen, M. J.; Plewa, M. J. The occurrence and toxicity of disinfection byproducts in European drinking waters in relation with the HIWATE epidemiology study Environ. Sci. Technol. 2012, 46 (21) 12120-12128
26. Levallois, P.; Gingras, S.; Marcoux, S.; Legay, C.; Catto, C.; Rodriguez, M.; Tardif, R. Maternal exposure to drinking-water chlorination by-products and small-for-gestational-age neonates Epidemiology 2012, 23 (2) 267-276
27. Colman, J.; Rice, G. E.; Wright, J. M.; Hunter, E. S., 3rd; Teuschler, L. K.; Lipscomb, J. C.; Hertzberg, R. C.; Simmons, J. E.; Fransen, M.; Osier, M.; Narotsky, M. G. Identification of developmentally toxic drinking water disinfection byproducts and evaluation of data relevant to mode of action Toxicol. Appl. Pharmacol. 2011, 254 (2) 100-126
28. Patelarou, E.; Kargaki, S.; Stephanou, E. G.; Nieuwenhuijsen, M.; Sourtzi, P.; Gracia, E.; Chatzi, L.; Koutis, A.; Kogevinas, M. Exposure to brominated trihalomethanes in drinking water and reproductive outcomes Occup. Environ. Med. 2011, 68 (6) 438-445
29. Grellier, J.; Bennett, J.; Patelarou, E.; Smith, R. B.; Toledano, M. B.; Rushton, L.; Briggs, D. J.; Nieuwenhuijsen, M. J. Exposure to disinfection by-products, fetal growth, and prematurity: A systematic review and meta-analysis Epidemiology 2010, 21 (3) 300-313
30. Savitz, D. A.; Singer, P. C.; Herring, A. H.; Hartmann, K. E.; Weinberg, H. S.; Makarushka, C. Exposure to drinking water disinfection by-products and pregnancy loss Am. J. Epidemiology 2006, 164 (11) 1043-1051
31. Krasner, S. W.; Weinberg, H. S.; Richardson, S. D.; Pastor, S. J.; Chinn, R.; Sclimenti, M. J.; Onstad, G. D.; Thruston, A. D., Jr. The occurrence of a new generation of disinfection by-products Environ. Sci. Technol. 2006, 40 (23) 7175-7185
32. Hua, G.; Reckhow, D. A.; Kim, J. Effect of bromide and iodide ions on the formation and speciation of disinfection byproducts during chlorination Environ. Sci. Technol. 2006, 40 (9) 3050-3056
33. Yang, M.; Zhang, X. Comparative developmental toxicity of new aromatic halogenated DBPs in a chlorinated saline sewage effluent to the marine polychaete Platynereis dumerilii Environ. Sci. Technol. 2013, 47 (19) 10868-10876
34. Liu, J.; Zhang, X. Comparative toxicity of new halophenolic DBPs in chlorinated saline wastewater effluents against a marine alga: Halophenolic DBPs are generally more toxic than haloaliphatic ones Water Res. 2014, 65C, 64-72
35. Kimura, S. Y.; Komaki, Y.; Plewa, M. J.; Mariñas, B. J. Chloroacetonitrile and N,2-dichloroacetamide formation from the reaction of chloroacetaldehyde and monochloramine in water Environ. Sci. Technol. 2013, 47, 12382-12390
36. Wagner, E. D.; Hsu, K. M.; Lagunas, A.; Mitch, W. A.; Plewa, M. J. Comparative genotoxicity of nitrosamine drinking water disinfection byproducts in Salmonella and mammalian cells Mutat. Res. 2012, 741, 109-115
37. Plewa, M. J.; Wagner, E. D.; Muellner, M. G.; Hsu, K. M.; Richardson, S. D., Comparative mammalian cell toxicity of N-DBPs and C-DBPs. In Occurrence, Formation, Health Effects and Control of Disinfection by-Products in Drinking Water; Karanfil, T.; Krasner, S. W.; Westerhoff, P.; Xie, Y., Eds.; American Chemical Society: Washington, D.C., 2008; Vol. 995, pp 36-50.
38. Shah, A. D.; Mitch, W. A. Halonitroalkanes, halonitriles, haloamides, and N-nitrosamines: A critical review of nitrogenous disinfection byproduct formation pathways Environ. Sci. Technol. 2012, 46 (1) 119-131
39. Bichsel, Y.; von Gunten, U. Formation of iodo-trihalomethanes during disinfection and oxidation of iodide containing waters Environ. Sci. Technol. 2000, 34 (13) 2784-2791
40. Ding, G.; Zhang, X. A picture of polar iodinated disinfection byproducts in drinking water by (UPLC/)ESI-tqMS Environ. Sci. Technol. 2009, 43 (24) 9287-9293
41. Weinberg, H. S.; Krasner, S. W.; Richardson, S. D.; Thruston, A. D., Jr. The Occurrence of Disinfection By-Products (DBPs) of Health Concern in Drinking Water: Results of a Nationwide DBP Occurrence Study, EPA/600/R02/068; U.S. Environmental Protection Agency National Exposure Research Laboratory: Athens, GA, 2002; pp 1-460.
42. Plewa, M. J.; Wagner, E. D.; Richardson, S. D.; Thruston, A. D., Jr.; Woo, Y. T.; McKague, A. B. Chemical and biological characterization of newly discovered iodoacid drinking water disinfection byproducts Environ. Sci. Technol. 2004, 38 (18) 4713-4722
43. Richardson, S. D.; Fasano, F.; Ellington, J. J.; Crumley, F. G.; Buettner, K. M.; Evans, J. J.; Blount, B. C.; Silva, L. K.; Waite, T. J.; Luther, G. W.; McKague, A. B.; Miltner, R. J.; Wagner, E. D.; Plewa, M. J. Occurrence and mammalian cell toxicity of iodinated disinfection byproducts in drinking water Environ. Sci. Technol. 2008, 42 (22) 8330-8338
44. Cancho, B.; Ventura, F.; Galceran, M.; Diaz, A.; Ricart, S. Determination, synthesis and survey of iodinated trihalomethanes in water treatment processes Water Res. 2000, 34 (13) 3380-3390
45. Richardson, S. D.; Thruston, A. D., Jr.; Rav-Acha, C.; Groisman, L.; Popilevsky, I.; Juraev, O.; Glezer, V.; McKague, A. B.; Plewa, M. J.; Wagner, E. D. Tribromopyrrole, brominated acids, and other disinfection byproducts produced by disinfection of drinking water rich in bromide Environ. Sci. Technol. 2003, 37 (17) 3782-3793
46. Krasner, S. W.; McGuire, M. J.; Jacangelo, J. G.; Patania, N. L.; Reagan, K. M.; Aieta, E. M. The occurrence of disinfection by-products in United-States drinking water J. Am. Water Work Assoc. 1989, 81 (8) 41-53
47. U. S. Environmental Protection Agency National primary drinking water regulations: Stage 2 disinfectants and disinfection byproducts rule Fed. Regist. 2006, 71 (2) 387-493
48. Seidel, C. J.; McGuire, M. J.; Scott, S. R.; Via, S. Have utilities switched to chloramines? J. Am. Water Works Assoc. 2005, 97 (10) 87-97
49. Bichsel, Y.; von Gunten, U. Oxidation of iodide and hypoiodous acid in the disinfection of natural waters Environ. Sci. Technol. 1999, 33 (22) 4040-4045
50. Muellner, M. G.; Wagner, E. D.; McCalla, K.; Richardson, S. D.; Woo, Y. T.; Plewa, M. J. Haloacetonitriles vs. regulated haloacetic acids: Are nitrogen containing DBPs more toxic? Environ. Sci. Technol. 2007, 41 (2) 645-651
51. Plewa, M. J.; Muellner, M. G.; Richardson, S. D.; Fasano, F.; Buettner, K. M.; Woo, Y. T.; McKague, A. B.; Wagner, E. D. Occurrence, synthesis and mammalian cell cytotoxicity and genotoxicity of haloacetamides: An emerging class of nitrogenous drinking water disinfection by-products Environ. Sci. Technol. 2008, 42 (3) 955-961
52. Jones, D. B.; Saglam, A.; Song, H.; Karanfil, T. The impact of bromide/iodide concentration and ratio on iodinated trihalomethane formation and speciation Water Res. 2012, 46, 11-20
53. Jones, D. B.; Saglam, A.; Triger, A.; Song, H.; Karanfil, T. I-THM formation and speciation: Preformed monochloramine versus prechlorination followed by ammonia addition Environ. Sci. Technol. 2011, 45 (2) 10429-10437
54. IPCC Summary for policymakers. In Climate Change 2013: The Physical Science Basis; Cambridge University Press: New York, 2013; p 28.
55. Watson, K.; Shaw, G.; Leusch, F. D.; Knight, N. L. Chlorine disinfection by-products in wastewater effluent: Bioassay-based assessment of toxicological impact Water Res. 2012, 46 (18) 6069-6083
56. Escher, B. I.; van Daele, C.; Dutt, M.; Tang, J. Y.; Altenburger, R. Most oxidative stress response in water samples comes from unknown chemicals: The need for effect-based water quality trigger values Environ. Sci. Technol. 2013, 47 (13) 7002-7011
57. Agus, E.; Voutchkov, N.; Sedlak, D. L. Disinfection by-products and their potential impact on the quality of water produced by desalination systems: A literature review Desalination 2009, 237 (1) 214-237
58. Wilson, J. M.; Van Briesen, J. M. Source water changes and energy extraction activities in the Monongahela River, 2009-2012 Environ. Sci. Technol. 2013, 47 (21) 12575-12582
59. Pals, J.; Ang, J.; Wagner, E. D.; Plewa, M. J. Biological mechanism for the toxicity of haloacetic acid drinking water disinfection byproducts Environ. Sci. Technol. 2011, 45, 5791-5797
60. Pals, J.; Attene-Ramos, M. S.; Xia, M.; Wagner, E. D.; Plewa, M. J. Human cell toxicogenomic analysis linking reactive oxygen species to the toxicity of monohaloacetic acid drinking water disinfection byproducts Environ. Sci. Technol. 2013, 47 (21) 12514-12523
61. Rivera-Nunez, Z.; Wright, J. M. Association of brominated trihalomethane and haloacetic acid exposure with fetal growth and preterm delivery in Massachusetts J. Occup. Environ. Med. 2013, 55 (10) 1125-1134
62. Eaton, A.; Clesceri, L.; Rice, E.; Greenberg, A. Standard Methods for the Examination of Water & Wastewater, 21 st ed.; AWWA, WEF, APHA: Baltimore, MD, 2005; p 4-67.
63. Richardson, S. D. XAD Resin Extraction of Disinfectant by-Products from Drinking Water: SOP-RSB-003.1- Revision No. 1; Environmental Protection Agency: Athens, GA, 2011.
64. Wagner, E. D.; Rayburn, A. L.; Anderson, D.; Plewa, M. J. Analysis of mutagens with single cell gel electrophoresis, flow cytometry, and forward mutation assays in an isolated clone of Chinese hamster ovary cells Environ. Mol. Mutagen. 1998, 32 (4) 360-368
65. Plewa, M. J.; Kargalioglu, Y.; Vankerk, D.; Minear, R. A.; Wagner, E. D. Mammalian cell cytotoxicity and genotoxicity analysis of drinking water disinfection by-products Environ. Mol. Mutagen. 2002, 40 (2) 134-142
66. Rundell, M. S.; Wagner, E. D.; Plewa, M. J. The comet assay: Genotoxic damage or nuclear fragmentation? Environ. Mol. Mutagen. 2003, 42 (2) 61-67
67. Tice, R. R.; Agurell, E.; Anderson, D.; Burlinson, B.; Hartmann, A.; Kobayashi, H.; Miyamae, Y.; Rojas, E.; Ryu, J. C.; Sasaki, Y. F. Single cell gel/comet assay: Guidelines for in vitro and in vivo genetic toxicology testing Environ. Mol. Mutagen. 2000, 35 (3) 206-221
68. Wagner, E. D.; Plewa, M. J. Microplate-based comet assay. In The Comet Assay in Toxicology; Dhawan, A.; Anderson, D., Eds.; Royal Society of Chemistry: London, 2009; pp 79-97.
69. Kumaravel, T. S.; Jha, A. N. Reliable Comet assay measurements for detecting DNA damage induced by ionising radiation and chemicals Mutat. Res. 2006, 605 (1-2) 7-16
70. Box, G. E. P.; Hunter, W. G.; Hunter, J. S. Statistics for Experimenters: An Introduction to Design, Data Analysis, and Model Building; Wiley & Sons Inc.: New York, NY., 1978.
71. Efron, B. Better bootstrap confidence intervals J. Am. Statis. Assoc. 1987, 82 (397) 171-185
72. Singh, K.; Xie, M. Bootstrap: A Statistical Method; Rutgers University, 2008; p 14.
73. Wu, Q. Y.; Li, Y.; Hu, H. Y.; Sun, Y. X.; Zhao, F. Y. Reduced effect of bromide on the genotoxicity in secondary effluent of a municipal wastewater treatment plant during chlorination Environ. Sci. Technol. 2010, 44 (13) 4924-4929
74. Malcolm, R. L.; MacCarthy, P. Quantitative evaluation of XAD-8 and XAD-4 resins used in tandem for removing organic solutes from water Environ. Int. 1992, 18, 597-607
75. Bond, T.; Henriet, O.; Goslan, E. H.; Parsons, S. A.; Jefferson, B. Disinfection byproduct formation and fractionation behavior of natural organic matter surrogates Environ. Sci. Technol. 2009, 43 (15) 5982-5989
76. Duirk, S. E.; Lindell, C.; Cornelison, C.; Kormos, J. L.; Ternes, T. A.; Attene-Ramos, M. S.; Osiol, J.; Wagner, E. D.; Plewa, M. J.; Richardson, S. D. Formation of toxic iodinated disinfection by-products from compounds used in medical imaging Environ. Sci. Technol. 2011, 45, 6845-6854
77. Richardson, S. D.; Thruston, A. D., Jr; Collette, T. W.; Patterson, K. S.; Lykins, B. W., Jr; Ireland, J. C. Identification of TiO2/UV disinfection byproducts in drinking water Environ. Sci. Technol. 1996, 30 (11) 3327-3334
78. Richardson, S. D.; Thruston, A. D., Jr; Krasner, S. W.; Weinberg, H. S.; Miltner, R. J.; Schenck, K. M.; Narotsky, M. G.; McKague, A. B.; Simmons, J. E. Integrated disinfection by-products mixtures research: Comprehensive characterization of water concentrates prepared from chlorinated and ozonated/postchlorinated drinking water J. Toxicol. Environ. Health A 2008, 71 (17) 1165-1186
79. Plewa, M. J.; Wagner, E. D.; Metz, D. H.; Kashinkunti, R.; Jamriska, K. J.; Meyer, M. Differential toxicity of drinking water disinfected with combinations of ultraviolet radiation and chlorine Environ. Sci. Technol. 2012, 46 (14) 7811-7817
80. Kumar, K.; Margerum, D. W. Kinetics and mechanism of general-acid-assisted oxidation of bromide by hypochlorite and hypochlorous acid Inorg. Chem. 1987, 26 (16) 2706-2711
81. Luh, J.; Marinas, B. J. Kinetics of bromochloramine formation and decomposition Environ. Sci. Technol. 2014, 48 (5) 2843-2852
82. Kristiana, I.; Gallard, H.; Joll, C.; Croue, J. P. The formation of halogen-specific TOX from chlorination and chloramination of natural organic matter isolates Water Res. 2009, 43 (17) 4177-4186
83. Zhai, H.; Zhang, X.; Zhu, X.; Liu, J.; Ji, M. Formation of brominated disinfection byproducts during chloramination of drinking water: New polar species and overall kinetics Environ. Sci. Technol. 2014, 48 (5) 2579-2588
84. Watson, K.; Farre, M. J.; Knight, N. Strategies for the removal of halides from drinking water sources, and their applicability in disinfection by-product minimisation: A critical review J. Environ. Manage. 2012, 110, 276-298
85. Allard, S.; Nottle, C. E.; Chan, A.; Joll, C.; von Gunten, U. Ozonation of iodide-containing waters: Selective oxidation of iodide to iodate with simultaneous minimization of bromate and I-THMs Water Res. 2013, 47 (6) 1953-1960