1932

Abstract

Arsenic is a naturally occurring hazardous element that is environmentally ubiquitous in various chemical forms. Upon exposure, the human body initiates an elimination pathway of progressive methylation into relatively less bioreactive and more easily excretable pentavalent methylated forms. Given its association with decreasing the internal burden of arsenic with ensuing attenuation of its related toxicities, biomethylation has been applauded for decades as a pure route of arsenic detoxification. However, the emergence of detectable trivalent species with profound toxicity has opened a long-standing debate regarding whether arsenic methylation is a detoxifying or bioactivating mechanism. In this review, we approach the topic of arsenic metabolism from both perspectives to create a complete picture of its potential role in the mitigation or aggravation of various arsenic-related pathologies.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-pharmtox-051921-020936
2023-01-20
2024-06-13
Loading full text...

Full text loading...

/deliver/fulltext/pharmtox/63/1/annurev-pharmtox-051921-020936.html?itemId=/content/journals/10.1146/annurev-pharmtox-051921-020936&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Parascandola J. 2012. King of Poisons: A History of Arsenic Dulles, VA: Potomac Books
    [Google Scholar]
  2. 2.
    Agency Toxic Subst. Dis. Regist. (ATSDR) 2007. Toxicological profile for arsenic Rep. ATSDR Atlanta, GA:
    [Google Scholar]
  3. 3.
    El-Ghiaty MA, El-Kadi AOS. 2021. Arsenic: various species with different effects on cytochrome P450 regulation in humans. EXCLI J 20:1184–242
    [Google Scholar]
  4. 4.
    Chen QY, Costa M. 2021. Arsenic: a global environmental challenge. Annu. Rev. Pharmacol. Toxicol. 61:47–63
    [Google Scholar]
  5. 5.
    Uthus EO. 2003. Arsenic essentiality: a role affecting methionine metabolism. J. Trace Elem. Exp. Med. 16:345–55
    [Google Scholar]
  6. 6.
    Mukhopadhyay R, Bhattacharjee H, Rosen BP. 2014. Aquaglyceroporins: generalized metalloid channels. Biochim. Biophys. Acta 1840:1583–91
    [Google Scholar]
  7. 7.
    Roggenbeck BA, Banerjee M, Leslie EM. 2016. Cellular arsenic transport pathways in mammals. J. Environ. Sci. 49:38–58
    [Google Scholar]
  8. 8.
    Luvonga C, Rimmer CA, Yu LL, Lee SB. 2020. Organoarsenicals in seafood: occurrence, dietary exposure, toxicity, and risk assessment considerations—a review. J. Agric. Food Chem. 68:943–60
    [Google Scholar]
  9. 9.
    Garbinski LD, Rosen BP, Chen J 2019. Pathways of arsenic uptake and efflux. Environ. Int. 126:585–97
    [Google Scholar]
  10. 10.
    Rahman MT, De Ley M. 2017. Arsenic induction of metallothionein and metallothionein induction against arsenic cytotoxicity. Rev. Environ. Contam. Toxicol. 240:151–68
    [Google Scholar]
  11. 11.
    Guo J, Xu W, Ma M. 2012. The assembly of metals chelation by thiols and vacuolar compartmentalization conferred increased tolerance to and accumulation of cadmium and arsenic in transgenic Arabidopsis thaliana. J. Hazard. Mater. 199–200 309–13
    [Google Scholar]
  12. 12.
    Moe B, Peng H, Lu X, Chen B, Chen LWL et al. 2016. Comparative cytotoxicity of fourteen trivalent and pentavalent arsenic species determined using real-time cell sensing. J. Environ. Sci. 49:113–24
    [Google Scholar]
  13. 13.
    Xue J, Zartarian V, Wang SW, Liu SV, Georgopoulos P. 2010. Probabilistic modeling of dietary arsenic exposure and dose and evaluation with 2003–2004 NHANES data. Environ. Health Perspect. 118:345–50
    [Google Scholar]
  14. 14.
    Lomax C, Liu WJ, Wu L, Xue K, Xiong J et al. 2012. Methylated arsenic species in plants originate from soil microorganisms. New Phytol 193:665–72
    [Google Scholar]
  15. 15.
    Challenger F. 1945. Biological methylation. Chem. Rev. 36:315–61
    [Google Scholar]
  16. 16.
    Hayakawa T, Kobayashi Y, Cui X, Hirano S. 2005. A new metabolic pathway of arsenite: Arsenic–glutathione complexes are substrates for human arsenic methyltransferase Cyt19. Arch. Toxicol. 79:183–91
    [Google Scholar]
  17. 17.
    Naranmandura H, Suzuki N, Suzuki KT. 2006. Trivalent arsenicals are bound to proteins during reductive methylation. Chem. Res. Toxicol. 19:1010–18
    [Google Scholar]
  18. 18.
    Watanabe T, Hirano S. 2013. Metabolism of arsenic and its toxicological relevance. Arch. Toxicol. 87:969–79
    [Google Scholar]
  19. 19.
    Cohen SM, Arnold LL, Eldan M, Lewis AS, Beck BD. 2006. Methylated arsenicals: the implications of metabolism and carcinogenicity studies in rodents to human risk assessment. Crit. Rev. Toxicol. 36:99–133
    [Google Scholar]
  20. 20.
    Hirano S. 2020. Biotransformation of arsenic and toxicological implication of arsenic metabolites. Arch. Toxicol. 94:2587–601
    [Google Scholar]
  21. 21.
    Natl. Res. Council 2013. Critical aspects of EPA's IRIS assessment of inorganic arsenic: interim report Rep. Natl. Res. Council Washington, DC:
    [Google Scholar]
  22. 22.
    Cohen SM, Arnold LL, Beck BD, Lewis AS, Eldan M. 2013. Evaluation of the carcinogenicity of inorganic arsenic. Crit. Rev. Toxicol. 43:711–52
    [Google Scholar]
  23. 23.
    Vahter M 1999. Variation in human metabolism of arsenic. Arsenic Exposure and Health Effects III WR Chappell, CO Abernathy, RL Calderon 267–79 Oxford, UK: Elsevier
    [Google Scholar]
  24. 24.
    Aposhian HV, Aposhian MM. 2006. Arsenic toxicology: five questions. Chem. Res. Toxicol. 19:1–15
    [Google Scholar]
  25. 25.
    North DW. 1992. Risk assessment for ingested inorganic arsenic: a review and status report. Environ. Geochem. Health 14:59–62
    [Google Scholar]
  26. 26.
    Chen B, Cao F, Yuan C, Lu X, Shen S et al. 2013. Arsenic speciation in saliva of acute promyelocytic leukemia patients undergoing arsenic trioxide treatment. Anal. Bioanal. Chem. 405:1903–11
    [Google Scholar]
  27. 27.
    Vahter M. 1999. Methylation of inorganic arsenic in different mammalian species and population groups. Sci. Prog. 82:Pt. 169–88
    [Google Scholar]
  28. 28.
    Cullen WR. 2014. Chemical mechanism of arsenic biomethylation. Chem. Res. Toxicol. 27:457–61
    [Google Scholar]
  29. 29.
    Rehman K, Naranmandura H. 2012. Arsenic metabolism and thioarsenicals. Metallomics 4:881–92
    [Google Scholar]
  30. 30.
    Borak J, Hosgood HD. 2007. Seafood arsenic: implications for human risk assessment. Regul. Toxicol. Pharmacol. 47:204–12
    [Google Scholar]
  31. 31.
    Naranmandura H, Carew MW, Xu S, Lee J, Leslie EM et al. 2011. Comparative toxicity of arsenic metabolites in human bladder cancer EJ-1 cells. Chem. Res. Toxicol. 24:1586–96
    [Google Scholar]
  32. 32.
    Raml R, Rumpler A, Goessler W, Vahter M, Li L et al. 2007. Thio-dimethylarsinate is a common metabolite in urine samples from arsenic-exposed women in Bangladesh. Toxicol. Appl. Pharmacol. 222:374–80
    [Google Scholar]
  33. 33.
    Mandal BK, Suzuki KT, Anzai K, Yamaguchi K, Sei Y. 2008. A SEC-HPLC-ICP MS hyphenated technique for identification of sulfur-containing arsenic metabolites in biological samples. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 874:64–76
    [Google Scholar]
  34. 34.
    Chen B, Cao F, Lu X, Shen S, Zhou J, Le XC. 2018. Arsenic speciation in hair and nails of acute promyelocytic leukemia (APL) patients undergoing arsenic trioxide treatment. Talanta 184:446–51
    [Google Scholar]
  35. 35.
    Rubin SSCDC, Alava P, Zekker I, Du Laing G, Van de Wiele T 2014. Arsenic thiolation and the role of sulfate-reducing bacteria from the human intestinal tract. Environ. Health Perspect. 122:817–22
    [Google Scholar]
  36. 36.
    Suzuki KT, Mandal BK, Katagiri A, Sakuma Y, Kawakami A et al. 2004. Dimethylthioarsenicals as arsenic metabolites and their chemical preparations. Chem. Res. Toxicol. 17:914–21
    [Google Scholar]
  37. 37.
    Bu N, Wang HY, Hao WH, Liu X, Xu S et al. 2011. Generation of thioarsenicals is dependent on the enterohepatic circulation in rats. Metallomics 3:1064–73
    [Google Scholar]
  38. 38.
    Yoshimura Y, Endo Y, Shimoda Y, Yamanaka K, Endo G. 2011. Acute arsine poisoning confirmed by speciation analysis of arsenic compounds in the plasma and urine by HPLC-ICP-MS. J. Occup. Health 53:45–49
    [Google Scholar]
  39. 39.
    Tsuji JS, Lennox KP, Watson HN, Chang ET. 2021. Essential concepts for interpreting the dose-response of low-level arsenic exposure in epidemiological studies. Toxicology 457:152801
    [Google Scholar]
  40. 40.
    Datta BK, Mishra A, Singh A, Sar TK, Sarkar S et al. 2010. Chronic arsenicosis in cattle with special reference to its metabolism in arsenic endemic village of Nadia district West Bengal India. Sci. Total Environ. 409:284–88
    [Google Scholar]
  41. 41.
    Lynch HN, Greenberg GI, Pollock MC, Lewis AS. 2014. A comprehensive evaluation of inorganic arsenic in food and considerations for dietary intake analyses. Sci. Total Environ. 496:299–313
    [Google Scholar]
  42. 42.
    Harrington CF, Brima EI, Jenkins RO. 2008. Biotransformation of arsenobetaine by microorganisms from the human gastrointestinal tract. Chem. Speciat. Bioavailab. 20:173–80
    [Google Scholar]
  43. 43.
    Taylor V, Goodale B, Raab A, Schwerdtle T, Reimer K et al. 2017. Human exposure to organic arsenic species from seafood. Sci. Total Environ. 580:266–82
    [Google Scholar]
  44. 44.
    Buchet JP, Lauwerys R, Roels H. 1981. Comparison of the urinary excretion of arsenic metabolites after a single oral dose of sodium arsenite, monomethylarsonate, or dimethylarsinate in man. Int. Arch. Occup. Environ. Health 48:71–79
    [Google Scholar]
  45. 45.
    Marafante E, Vahter M, Norin H, Envall J, Sandström M et al. 1987. Biotransformation of dimethylarsinic acid in mouse, hamster and man. J. Appl. Toxicol. 7:111–17
    [Google Scholar]
  46. 46.
    Shen S, Li XF, Cullen WR, Weinfeld M, Le XC. 2013. Arsenic binding to proteins. Chem. Rev. 113:7769–92
    [Google Scholar]
  47. 47.
    Dopp E, Hartmann LM, von Recklinghausen U, Florea AM, Rabieh S et al. 2005. Forced uptake of trivalent and pentavalent methylated and inorganic arsenic and its cyto-/genotoxicity in fibroblasts and hepatoma cells. Toxicol. Sci. 87:46–56
    [Google Scholar]
  48. 48.
    Bertolero F, Pozzi G, Sabbioni E, Saffiotti U. 1987. Cellular uptake and metabolic reduction of pentavalent to trivalent arsenic as determinants of cytotoxicity and morphological transformation. Carcinogenesis 8:803–8
    [Google Scholar]
  49. 49.
    Kurosawa H, Shimoda Y, Miura M, Kato K, Yamanaka K et al. 2016. A novel metabolic activation associated with glutathione in dimethylmonothioarsinic acid (DMMTAV)-induced toxicity obtained from in vitro reaction of DMMTAV with glutathione. J. Trace Elem. Med. Biol. 33:87–94
    [Google Scholar]
  50. 50.
    Delnomdedieu M, Basti MM, Otvos JD, Thomas DJ. 1994. Reduction and binding of arsenate and dimethylarsinate by glutathione: a magnetic resonance study. Chem. Biol. Interact. 90:139–55
    [Google Scholar]
  51. 51.
    Sakurai T, Qu W, Sakurai MH, Waalkes MP. 2002. A major human arsenic metabolite, dimethylarsinic acid, requires reduced glutathione to induce apoptosis. Chem. Res. Toxicol. 15:629–37
    [Google Scholar]
  52. 52.
    Hughes MF. 2002. Arsenic toxicity and potential mechanisms of action. Toxicol. Lett. 133:1–16
    [Google Scholar]
  53. 53.
    Naranmandura H, Ogra Y, Iwata K, Lee J, Suzuki KT et al. 2009. Evidence for toxicity differences between inorganic arsenite and thioarsenicals in human bladder cancer cells. Toxicol. Appl. Pharmacol. 238:133–40
    [Google Scholar]
  54. 54.
    Ochi T, Kita K, Suzuki T, Rumpler A, Goessler W, Francesconi KA. 2008. Cytotoxic, genotoxic and cell-cycle disruptive effects of thio-dimethylarsinate in cultured human cells and the role of glutathione. Toxicol. Appl. Pharmacol. 228:59–67
    [Google Scholar]
  55. 55.
    Miller CG, Schmidt EE. 2019. Disulfide reductase systems in liver. Br. J. Pharmacol. 176:532–43
    [Google Scholar]
  56. 56.
    Wang Z, Zhang H, Li XF, Le XC. 2007. Study of interactions between arsenicals and thioredoxins (human and E. coli) using mass spectrometry. Rapid Commun. Mass Spectrom. 21:3658–66
    [Google Scholar]
  57. 57.
    Lin S, Del Razo LM, Styblo M, Wang C, Cullen WR, Thomas DJ. 2001. Arsenicals inhibit thioredoxin reductase in cultured rat hepatocytes. Chem. Res. Toxicol. 14:305–11
    [Google Scholar]
  58. 58.
    Lu J, Chew EH, Holmgren A. 2007. Targeting thioredoxin reductase is a basis for cancer therapy by arsenic trioxide. PNAS 104:12288–93
    [Google Scholar]
  59. 59.
    Styblo M, Serves SV, Cullen WR, Thomas DJ. 1997. Comparative inhibition of yeast glutathione reductase by arsenicals and arsenothiols. Chem. Res. Toxicol. 10:27–33
    [Google Scholar]
  60. 60.
    Bergquist ER, Fischer RJ, Sugden KD, Martin BD. 2009. Inhibition by methylated organo-arsenicals of the respiratory 2-oxo-acid dehydrogenases. J. Organomet. Chem. 694:973–80
    [Google Scholar]
  61. 61.
    Paul DS, Harmon AW, Devesa V, Thomas DJ, Stýblo M. 2007. Molecular mechanisms of the diabetogenic effects of arsenic: inhibition of insulin signaling by arsenite and methylarsonous acid. Environ. Health Perspect. 115:734–42
    [Google Scholar]
  62. 62.
    Huang M, Douillet C, Stýblo M. 2019. Arsenite and its trivalent methylated metabolites inhibit glucose-stimulated calcium influx and insulin secretion in murine pancreatic islets. Arch. Toxicol. 93:2525–33
    [Google Scholar]
  63. 63.
    Witkiewicz-Kucharczyk A, Bal W. 2006. Damage of zinc fingers in DNA repair proteins, a novel molecular mechanism in carcinogenesis. Toxicol. Lett. 162:29–42
    [Google Scholar]
  64. 64.
    Zhou X, Sun X, Mobarak C, Gandolfi AJ, Burchiel SW et al. 2014. Differential binding of monomethyl-arsonous acid compared to arsenite and arsenic trioxide with zinc finger peptides and proteins. Chem. Res. Toxicol. 27:690–98
    [Google Scholar]
  65. 65.
    Walter I, Schwerdtle T, Thuy C, Parsons JL, Dianov GL, Hartwig A. 2007. Impact of arsenite and its methylated metabolites on PARP-1 activity, PARP-1 gene expression and poly(ADP-ribosyl)ation in cultured human cells. DNA Repair 6:61–70
    [Google Scholar]
  66. 66.
    Schwerdtle T, Walter I, Hartwig A. 2003. Arsenite and its biomethylated metabolites interfere with the formation and repair of stable BPDE-induced DNA adducts in human cells and impair XPAzf and Fpg. DNA Repair 2:1449–63
    [Google Scholar]
  67. 67.
    Piatek K, Schwerdtle T, Hartwig A, Bal W. 2008. Monomethylarsonous acid destroys a tetrathiolate zinc finger much more efficiently than inorganic arsenite: mechanistic considerations and consequences for DNA repair inhibition. Chem. Res. Toxicol. 21:600–6
    [Google Scholar]
  68. 68.
    Spuches AM, Wilcox DE. 2008. Monomethylarsenite competes with Zn2+ for binding sites in the glucocorticoid receptor. J. Am. Chem. Soc. 130:8148–49
    [Google Scholar]
  69. 69.
    Kligerman AD, Doerr CL, Tennant AH. 2005. Oxidation and methylation status determine the effects of arsenic on the mitotic apparatus. Mol. Cell. Biochem. 279:113–21
    [Google Scholar]
  70. 70.
    Bustaffa E, Stoccoro A, Bianchi F, Migliore L. 2014. Genotoxic and epigenetic mechanisms in arsenic carcinogenicity. Arch. Toxicol. 88:1043–67
    [Google Scholar]
  71. 71.
    Zhang Q, Li Y, Liu J, Wang D, Zheng Q, Sun G. 2014. Differences of urinary arsenic metabolites and methylation capacity between individuals with and without skin lesions in Inner Mongolia, Northern China. Int. J. Environ. Res. Public Health 11:7319–32
    [Google Scholar]
  72. 72.
    Steinmaus C, Yuan Y, Kalman D, Rey OA, Skibola CF et al. 2010. Individual differences in arsenic metabolism and lung cancer in a case-control study in Cordoba, Argentina. Toxicol. Appl. Pharmacol. 247:138–45
    [Google Scholar]
  73. 73.
    Tam GK, Charbonneau SM, Bryce F, Pomroy C, Sandi E 1979. Metabolism of inorganic arsenic (74As) in humans following oral ingestion. Toxicol. Appl. Pharmacol. 50:319–22
    [Google Scholar]
  74. 74.
    Valenzuela OL, Borja-Aburto VH, Garcia-Vargas GG, Cruz-Gonzalez MB, Garcia-Montalvo EA et al. 2005. Urinary trivalent methylated arsenic species in a population chronically exposed to inorganic arsenic. Environ. Health Perspect. 113:250–54
    [Google Scholar]
  75. 75.
    Antonelli R, Shao K, Thomas DJ, Sams R 2nd, Cowden J. 2014. AS3MT, GSTO, and PNP polymorphisms: impact on arsenic methylation and implications for disease susceptibility. Environ. Res. 132:156–67
    [Google Scholar]
  76. 76.
    Vahter M, Marafante E. 1983. Intracellular interaction and metabolic fate of arsenite and arsenate in mice and rabbits. Chem. Biol. Interact. 47:29–44
    [Google Scholar]
  77. 77.
    Chi L, Gao B, Tu P, Liu CW, Xue J et al. 2018. Individual susceptibility to arsenic-induced diseases: the role of host genetics, nutritional status, and the gut microbiome. Mamm. Genome 29:63–79
    [Google Scholar]
  78. 78.
    Eichstaedt CA, Antao T, Cardona A, Pagani L, Kivisild T, Mormina M. 2015. Positive selection of AS3MT to arsenic water in Andean populations. Mutat. Res. 780:97–102
    [Google Scholar]
  79. 79.
    Li J, Packianathan C, Rossman TG, Rosen BP. 2017. Nonsynonymous polymorphisms in the human AS3MT arsenic methylation gene: implications for arsenic toxicity. Chem. Res. Toxicol. 30:1481–91
    [Google Scholar]
  80. 80.
    Lu J, Hu S, Wang W, Li J, Dong Z et al. 2018. AS3MT polymorphisms, arsenic metabolism, and the hematological and biochemical values in APL patients treated with arsenic trioxide. Toxicol. Sci. 166:219–27
    [Google Scholar]
  81. 81.
    Pu YS, Yang SM, Huang YK, Chung CJ, Huang SK et al. 2007. Urinary arsenic profile affects the risk of urothelial carcinoma even at low arsenic exposure. Toxicol. Appl. Pharmacol. 218:99–106
    [Google Scholar]
  82. 82.
    Lin YC, Chen WJ, Huang CY, Shiue HS, Su CT et al. 2018. Polymorphisms of arsenic (+3 oxidation state) methyltransferase and arsenic methylation capacity affect the risk of bladder cancer. Toxicol. Sci. 164:328–38
    [Google Scholar]
  83. 83.
    Hernández A, Xamena N, Surrallés J, Sekaran C, Tokunaga H et al. 2008. Role of the Met287Thr polymorphism in the AS3MT gene on the metabolic arsenic profile. Mutat. Res. 637:80–92
    [Google Scholar]
  84. 84.
    Lindberg AL, Kumar R, Goessler W, Thirumaran R, Gurzau E et al. 2007. Metabolism of low-dose inorganic arsenic in a central European population: influence of sex and genetic polymorphisms. Environ. Health Perspect. 115:1081–86
    [Google Scholar]
  85. 85.
    Agusa T, Iwata H, Fujihara J, Kunito T, Takeshita H et al. 2009. Genetic polymorphisms in AS3MT and arsenic metabolism in residents of the Red River Delta, Vietnam. Toxicol. Appl. Pharmacol. 236:131–41
    [Google Scholar]
  86. 86.
    Hernández A, Paiva L, Creus A, Quinteros D, Marcos R 2014. Micronucleus frequency in copper-mine workers exposed to arsenic is modulated by the AS3MT Met287Thr polymorphism. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 759:51–55
    [Google Scholar]
  87. 87.
    Sampayo-Reyes A, Hernández A, El-Yamani N, López-Campos C, Mayet-Machado E et al. 2010. Arsenic induces DNA damage in environmentally exposed Mexican children and adults. Influence of GSTO1 and AS3MT polymorphisms. Toxicol. Sci. 117:63–71
    [Google Scholar]
  88. 88.
    Valenzuela OL, Drobná Z, Hernández-Castellanos E, Sánchez-Peña LC, García-Vargas GG et al. 2009. Association of AS3MT polymorphisms and the risk of premalignant arsenic skin lesions. Toxicol. Appl. Pharmacol. 239:200–7
    [Google Scholar]
  89. 89.
    Drobná Z, Del Razo LM, García-Vargas GG, Sánchez-Peña LC, Barrera-Hernández A et al. 2013. Environmental exposure to arsenic, AS3MT polymorphism and prevalence of diabetes in Mexico. J. Expo. Sci. Environ. Epidemiol. 23:151–55
    [Google Scholar]
  90. 90.
    Beebe-Dimmer JL, Iyer PT, Nriagu JO, Keele GR, Mehta S et al. 2012. Genetic variation in glutathione S-transferase omega-1, arsenic methyltransferase and methylene-tetrahydrofolate reductase, arsenic exposure and bladder cancer: a case-control study. Environ. Health 11:43
    [Google Scholar]
  91. 91.
    Bozack AK, Saxena R, Gamble MV. 2018. Nutritional influences on one-carbon metabolism: effects on arsenic methylation and toxicity. Annu. Rev. Nutr. 38:401–29
    [Google Scholar]
  92. 92.
    Abuawad A, Bozack AK, Saxena R, Gamble MV. 2021. Nutrition, one-carbon metabolism and arsenic methylation. Toxicology 457:152803
    [Google Scholar]
  93. 93.
    Sijko M, Kozłowska L. 2021. Influence of dietary compounds on arsenic metabolism and toxicity. Part II—human studies. Toxics 9:259
    [Google Scholar]
/content/journals/10.1146/annurev-pharmtox-051921-020936
Loading
/content/journals/10.1146/annurev-pharmtox-051921-020936
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error