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IJRPC 2016, 6(2), 192-206 Hussein M Abdel-Fattah et al. ISSN: 22312781

INTERNATIONAL JOURNAL OF RESEARCH IN PHARMACY AND CHEMISTRY

Available online at www.ijrpc.com Review Article

A REVIEW ON THE CHEMICAL ANALYSIS OF AND ITS REMOVAL FROM REAL AND BIOLOGICAL SAMPLES Yousry M Issa, Hussein M Abdel-Fattah* and Nahla B Abdel-Moniem Chemistry Department, Faculty of Science, Cairo University, Giza, 12613, Egypt.

ABSTRACT Tellurium demonstrates properties similar to those of elements known to be toxic to humans, and has applications in industrial processes that are rapidly growing in importance and scale. It is also considered to be extremely toxic, and clinical manifestations of toxicity are observed at very low concentrations. Therefore, there are several methods interested in determination and removal of tellurium in its environmental and biological samples. In this review, we will focus on the protocols that deal with determination, speciation and removal of tellurium in real and biological samples. This includes volumetric, spectral, chromatographic and potentiometric methods, etc. This review also highlights ongoing research activities and presents the challenges that should be addressed in the future.

Keywords: Tellurium, Analysis, Removal, Speciation .

1. INTRODUCTION --tellurium compound Tellurium (Te) is a metalloid element used for optical storage on digital video discs7. belonging to the VIA group of the periodic There is some interest in the use of radioactive table that shares some chemical properties tellurium to treat thyroid cancer, and Te- with elements such as , , and containing antitumor agents have been selenium1. Tellurium was discovered in 1782 developed8. and was so called from the Latin word for Although tellurium is not an essential element earth, tellus. The abundance of tellurium in and is relatively rare in the environment, it is earth’s crust is 0.01 ppm .It occurs mainly as also considered to be extremely toxic, and tellurides with gold, , , and bismuth2. clinical manifestations of toxicity are observed Tellurium occurs naturally in a number of at very low concentrations2. inorganic forms, including telluride, Tellurium can be accumulated mainly in the and . kidneys, heart, liver, spleen, bone, and lung Although tellurium is not widely used, it is and its threshold should not excess 2.5 required in a number of important industrial mg/kg2, if exceed it could induce the applications3. Together with elements, such as degeneracy of the liver and kidneys9. In As, Sb, and Se, it plays a particular role in the humans, tellurium is partly metabolized into manufacturing of semiconductors and other dimethyl telluride, (CH3)2Te gas which is a electronic components. It is a component of characteristic feature of exposure, and gives a special alloys, where it improves hardness and pungent -like odor to breath, excreta, and resistance to corrosion, and also of certain the viscera. The main target sites for Te glasses. Tellurium compounds are used in the toxicity are the kidney, nervous system, skin, rubber industries, the manufacture of batteries, and the fetus (hydrocephalus). The emission and are found in fairly large amounts in the of inorganic tellurium compounds in the human body4,5. Tellurium improves the environment may create serious problems due machinability of and stainless steel and to the acute and chronic toxicity of this its addition to lead decreases the corrosive element. The most obvious sign of Te action of sulfuric on lead and improves its exposure is the garlic odor and other mild hardness6. New applications include a symptoms include dry mouth, metallic taste,

192 IJRPC 2016, 6(2), 192-206 Hussein M Abdel-Fattah et al. ISSN: 22312781

and somnolence10. Furthermore, tellurium’s special attention to development methods for toxicity, bioavailability and environmental tellurium speciation analysis. Several transport mechanism highly depend on its analytical techniques have been applied for chemical form and . For speciation of tellurium in real and biological example, tellurite is 10 times more toxic than samples. The most important are volumetric, tellurate11. The of tellurium, spectral, chromatographic and potentiometric 2- particularly tellurite (TeO3 or Te(IV), are methods, these methods are described below. highly toxic for most microorganisms12. The main reason for metal toxicity is oxidative 2. VOLUMETRIC METHODS damage of proteins, DNA, and lipids. It has Masson24 studied a procedure for titration of been proposed that this toxicity results from an selenite, tellurite and arsenate with silver ability of Te(IV) to act as a strong oxidizing nitrate, and its application in the determination agent13, as Te(IV) directly interacts with and of organic and organometallic compounds. oxidizes cellular thiol groups14,15. Te(IV) has Decomposition is carried out either by oxygen- also been implicated in redox reactions flask combustion or by wet digestion with involving the respiratory chain16. Recent sulphuric and nitric . Pure silver wire was reports favor an oxidative mode of action; used as an indicator electrode. The analysis is Te(IV) increases the production of reactive completed by argentometric titration, at pH 8- oxygen species (ROS) in vitro as well as in 8.5, of the selenite, tellurite or arsenate vivo, and increases protein carbonylation17. formed. Halogens can often be determined It has long been known that different bacterial simultaneously, and procedures are given for species vary in their tolerance to Te(IV), which dealing with metal-containing compounds. 2- has prompted the inclusion of TeO3 in a Results obtained are within the usual limits for variety of selective bacteriological tests18. microanalysis (+0.3%). However, tellurite-resistant bacteria do exist in A direct cerimetric method for determination nature and they often reduce tellurite to its Te(IV) was developed by Dindi and Reddy25. elemental less toxic form Te0 that is The sample (containing 10 to 100 mg of Te) -1 accumulated as black deposits inside the was mixed with H2SO4 (to give a 1 to 5 mol L 19,20 cell . Resistant cells grow as black colonies when diluted to 50 mL) and with RuCl3 as 2- on relatively high concentrations of TeO3 . catalyst to give a mole ratio of Te(IV) to Ru of Tellurite has been used for 80 years for the ≥ 800:1. The mixture was heated to ~100 ºC isolation of pathogens including and titrated slowly with stirring with a standard Corynebacterium diphtheriae, Staphylococcus solution of Ce(NH4)4(SO4)4. The end-point was aureus, Vibrio cholerae and Shigella spp. 21,22. the appearance of the first persistent pale Also tellurite is used for selection of yellow colour. The method can also be carried -1 verocytotoxigenic Escherichia coli 0157, where out in 1 to 2 mol L HNO3 with + tellurite allow the growth of VT E. coli 0157 Ce(NH4)2(NO3)6. The coefficient of variation (n and Shigella sonnei but partially or completely = 10) obtained with the use of H2SO4 or HNO3 inhibited the growth of other strains of E. coli were 0.21 and 0.15%, respectively. No 23. interference occurred in either media from Thus, Te demonstrates properties similar to Cu(II), AgI and Cl- up to 2.5, 60 and 10 mmol those of elements known to be toxic to L-1, respectively, and Pb(II) does not interfere -1 humans, and has applications in industrial at up to 50 mmol L in HNO3 medium. All processes that are rapidly growing in other that can be oxidized with Ce(IV) importance and scale. It is relevant, therefore, interfere. This method has been extended to to consider the Te physiology, toxicity, and the analysis of tellurate-tellurite mixtures by methods for monitoring the element in converting Te(VI) to Te(IV) by heating with biological and environmental specimens. For conc. HCl. these reasons, analytical chemists have paid

Table 1: Literature data survey for volumetric determination of tellurium Technique used Form of Te Linear range LOD Titrant pH Type of samples Ref. Argentometric Te(VI) and Organic and organometallic ------AgNO 8.0-8.5 [24] titration Te(IV) 3 compounds Ce(NH ) (SO ) Cerimetric titration Te(IV) ------4 4 4 Acidic Tellurate-tellurite mixture [25] 4

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3. SPECTRAL METHODS absorption spectrophotometry after separation Spectrophotometric method for determination and enrichment with “thiol cotton” and hydride of tellurium as iodotellurite complex was generation has been established29. The studied by Johnson and Kewan26. Iodotellurite sorption behavior of various oxidation states of complex is soluble, highly colored and shows , antimony, and tellurium, and absorption maxima at 335 and 285 nm. In the conditions of quantitative sorption and mixtures of 0.15 to 0.40 mol L-1 hydrochloric desorption of these species were studied. The acid and 0.25 to 0.40 mol L-1 iodide, procedures for reducing species from higher the absorption of the iodotellurite complex at oxidation states were optimized. Interferences 335 nm follows Beer’s law in the range 0.2 to 2 from other species and their elimination were µg mL-1of tellurium. Errors from the side investigated. The selectivity of the procedure reaction involving iodine formation by air for the determination of species in higher and oxidation of iodide are avoided by using low- lower oxidation states was examined. This actinic glassware and by making readings method was applied in determination of soon after mixing the reagents. also arsenic, antimony, selenium and tellurium in forms a colored iodo complex and must be , in the range from pg mL-1 to ng mL-1. removed. Selenite is reduced to colloidal The recoveries for added spikes were in the selenium by the iodide. Fe(III) and Cu(II) ions range 90-110%, with coefficients of variation in oxidize iodide and thus interfere. Convenient the range 3-8%. separations from each of these are described. For the quantitative determination of tellurite in Nitrate, sulfate, (II), , , biological media, Turner et al.30 described a (II), and (II) ions do not interfere. method depending on the use of This method can be used in metallurgy, diethyldithiocarbamate. In earlier protocols, biological science, and industrial hygiene. diethyldithiocarbamate reacted with tellurite Walper et al.27 developed a method for the and the resulting complex was extracted into quantitative determination of tellurite in organic solvents before spectrophotometric bacteriological culture medium depending on determination. In this study, Tellurite thioacetamide. Tellurite can be reduced to containing fermentation broth (100 µL) was elemental tellurium with the action of mixed with 0.5 mol L-1 Tris-HCl (pH 7.0, 300 sulfide and readily forms colloidal solutions. µL) and 10 mmol L-1 diethyldithiocarbamate Thioactamide was used as a convenient (100 µL) and diluted to 500 µL with H2O to source of hydrogen sulfide. The tellurite form a yellow colloidal solution. The solutions after reduction were measured absorbance of the aqueous yellow solution spectrophotometry at wavelength 350 nm. the was measured at 340 nm. Beer`s law was results obey Beer’s law is the range 1-10 µg obeyed from 1 to 50 µg mL-1 (4 to 200 µmol L- mL-1 of tellurite. The coefficient of variation for 1) of tellurite (ε= 5080). Decrease of this method was 1.7%; the percentage error absorbance caused by solution degradation was 3.0. was 27% after 2 hours, absorbance should, Thompson et al.28 studied a procedure for the therefore, be measured in 4 hours. The simultaneous determination of arsenic, method was applied to Escherichia coli. antimony, bismuth, selenium and tellurium by The occupational exposure to Te was studied generation of their gaseous hydrides and by Tylor [2]. Hydride generation atomic introduction of these hydrides into an absorption spectrometry provides accurate, inductively coupled plasma source where the precise, and timely measurements results. The atomic line emission from the elements is measurement occurred at 214.3 nm. Animal detected. The effect of different plasma-torch studies suggest that up to 25% of orally assemblies on the detection limits attainable administered tellurium is absorbed in the gut. has been studied and suitable compromise There is a biphasic elimination from the conditions have been established for the circulation with loss of about 50% within a simultaneous generation of the hydrides of the short period, t1/2= 0.81 d, and slower analyte elements and their determination by elimination of the residual Te, t1/2 = 12.9 d. The optical emission spectrometry in the plasma results showed that the minimum fatal dose of -1 source. Detection limits of 1 ng mL or below Na2TeO3 is 2.25-2.50 mg/kg while Na2TeO4 is for aqueous solutions of the elements studied 20-30 mg/kg, so tellurite is more toxic approx have been obtained under the conditions 10-fold than tellurate. employed to allow their determination in Najafi et al.31 developed a method for samples of interest in geochemistry. speciation and determination of Te(IV) and A method for determination of trace As(III) and Te(VI). The method depends on dispersive As(V), Sb(III) and Sb(V), Se(IV) and Se(VI), liquid-liquid microextraction combined with Te(IV) and Te(V1) in water by atomic- electrothermal atomic absorption spectrometry

194 IJRPC 2016, 6(2), 192-206 Hussein M Abdel-Fattah et al. ISSN: 22312781 using as permanent modifier. Under 200 μg L-1, with a correlation coefficient (r2) of acidic conditions (pH 1), only Te(IV) can form 0.997 and a limit of detection (S/N=3) of 2 μg a complex with ammonium pyrrolidine L-1. The results showed that the method dithiocarbamate (APDC) and, therefore, be provided superior performance with respect to extracted into fine droplets of tolerance to various coexisting ions such as tetrachloride (extraction solvent) which are Mg2+, Ca2+, Fe3+, Zn2+, Pb2+, As3+, Ge2+, and dispersed with ethanol into the water sample Hg2+. The proposed method can be applied in solution. After centrifugation, Te(IV) was detecting tellurium in environmental and determined in the sedimented organic phase biological samples. while Te(VI) remained in the aqueous phase. Zhang et al.34 proposed a simultaneous multi- Total inorganic tellurium was determined after channel hydride generation atomic the reduction of the Te(VI) to Te(IV). Te(VI) fluorescence spectrometry (HG-AFS) method was calculated as the difference between the for determination of total arsenic (As), total measured total inorganic tellurium and Te(IV) bismuth (Bi), total tellurium (Te) and total content. The effective parameters for selenium (Se) in tea leaves. The operating improving the efficiency of microextraction parameters of self-made multi-channel HG- process were investigated by using AFS were optimized, including negative high experimental and central composite designs. voltage of photomultiplier tube (PMT), the flow Under optimal conditions the enrichment factor rates of carrier and shield gas, observation was 125 and the calibration graph was linear height and lamp currents. The conditions of in the range of 0.015-1.0 ng mL-1 with hydride generation for As, Bi, Te and Se were detection limit and characteristic mass of studied in details. Under optimal conditions, 0.004 ng mL-1 and 0.033 pg, respectively. The the method detection limits (MDL) for As, Bi, relative standard deviation for 0.5 ng mL-1 of Te and Se in tea leaves were 0.0152, 0.0080, tellurium measurement was 3.6% (n=6) at ash 0.0022 and 0.0068 µg/g, respectively. The and atomization temperature, 900 and 2600 proposed method was applied to the °C, respectively. The recoveries of spiked simultaneous determination of As, Bi, Te and Te(IV) and Te(VI) to the environmental water Se in various tea leaves and the spike samples were 89.6-101.3% and 96.6-99.1%, recoveries were in the range of 90-103%. The respectively. The accuracy is also evaluated accuracy of method was validated by by applying the proposed method to certified analyzing a tea certified reference material. reference material (NIST SRM 1643e), for The obtained values were consistent with the which the result was in a good agreement with certified ones. the certified values reported for this CRM An electrolysis process for the (95% confidence level). preconcentration of selenium (IV) and tellurium Molina et al.32 described a chemical method (IV) is reported35. Where, Electrodeposition for tellurite quantification. The procedure is technique used for sample preparation in X- based on the NaBH4 mediated reduction of ray fluorescence spectrometry with 2- TeO3 followed by the spectrophotometric advantages of low cost, high sensitivity, and determination of elemental tellurium in minimal interferences. The analytes were solution. The method was applied in culture electrodeposited on a polished substrate of media and showed reproducible results, stable high purity copper, which was rinsed with at different pH values, and exhibits linearity deionized water, dried, and directly analyzed over a broad range of tellurite concentrations. by x-ray fluorescence. The influence of Hydride generation was inducted into the concomitant metal ions, electrodeposition chemiluminescence for the determination of voltage, pH, and electrolyte concentration on tellurium (IV) by Luo et al.33. The experiment the deposition efficiency was investigated. The exhibited that the strong chemiluminescence reproducibility of determination was 2.4% for emission can be obtained during the reaction selenium (IV) and 1.9% for tellurium (IV) (n = between hydrogen telluride and luminol in 7). The detection limits for the measurement of basic medium, and a novel sensitive hydride selenium (IV) and tellurium (IV) were 0.44 and generation chemiluminescence (HG-CL) 0.57 µg L−1, respectively. The method was methodology for the determination of tellurium validated by analyzing certified reference was proposed. Under the optimized materials and applied to the determination of conditions, the linear range of CL intensity trace selenium and tellurium in environmental versus concentration of tellurium (IV) was 10– water samples with satisfactory results.

195 IJRPC 2016, 6(2), 192-206 Hussein M Abdel-Fattah et al. ISSN: 22312781

Table 2: Literature data survey on spectral methods for tellurium determination Form of Linear λ Type of Technique used LOD Reagent pH max ɛ Ref Te range (nm) samples 0.2-2 µg Acidic Spectrophotometry Te(IV) -1 --- KI 335 -- Pure solution [26] mL (HCl) 1-10 µg Bacteriological Spectrophotometry Te(IV) -1 -- Thioacetamide Neutral 350 -- [27] mL culture medium ICP-emission [28] spectrometry Thiol cotton Te(IV) -1 0.008 Hydride generation- pg mL to - (separation) and -1 ng mL 3.0 214.2 --- Water [29] AAS ng mL 1 potassium Te(VI) borohydride 1 to 50 µg Diethyldithiocarba Biological Spectrophotometry Te(IV) --- 7.0 340 5080 [30] mL-1 mate media (E coli) Biological Te(IV) Hydride generation- Alkaline samples(blood, and ------214.3 --- [2] AAS borohydride NaOH urine Te(VI) membranes) Palladium as Dispersive liquid– Te(IV) 0.004 permanent 0.015-1 ng - liquid extraction - and -1 ng mL modifier 1.0 214.3 --- Water samples [31] mL 1 AAS Te(VI) Sodium borohydride pH 1-200 µg - Spectrophotometry Te(IV) --- NaBH depentan 500 --- Culture media [32] mL-1 4 t Hydride generation- - Environmental 10-200 μg 2 μg L KBH4 chemiluminescence Te(IV) -1 1 11.5 ------and biological [33] L Luminol (HG-CL) samples Hydride generation Potassium atomic fluorescence 0.1-10 ng 0.0022 Te(IV) -1 tetrahydroborate ------Tea leaves [34] spectrometry (HG- mL µg/g KBH AFS) 4 Electrodeposition 0.57 of tellurium on a Environmental X-Ray Fluorescence Te(IV) --- −1 ------[35] µg L polished substrate water samples of copper

4. SEPARATION AND hydroxide solution, the distribution coefficient CHROMATOGRAPHIC METHODS of sulfite decreased, while that of tellurite and Lederer et al.36 examined the eluation of selenite increased at first and then decreased. tellurite and selenite on paper impregnated This assay provided a complete separation of with dowex-50 in presence of numerous acids. tellurite, selenite by the anion exchange using It was possible to relate RM value [RM = an alkaline eluant. 38 log(1/RF-1)] with the pH of the eluting acid. Yoshida and Hida described an This relationship can also be used for the isotachophoresis method for separation of determination of the charge on . selenate, selenite, tellurate and tellurite ions. The separation of tellurite, selenite and sulfite The effect of the pH of the leading electrolyte ions by anion exchange resins was carried out and the type of counter-ion on the separation by Iguch37. The distribution coefficients of of the cited anions was examined. Ion-pairing tellurite, selenite and sulfite in neutral nitrate equilibria between the anions and the Ni(II)- solution and alkaline hydroxide solution were 1,10-phenanthroline and Co(III)- measured and the results suggest the ethylenediamine complexes were the basis of - presence of an acid salt ion HXO3 in neutral the separation. solution. By the addition of ammonia to the Selenite and tellurite were separated using eluant solution, the distribution coefficient of extraction chromatography by Hu et al.39. The these salts in nitrate solution was increased, separation depends on the use of N263 (a but in hydroxide solution it was decreased. commercial C8 to C10 However, by the addition of ethanol to the trialkylmethylammonium chloride) as eluant solution that containing nitrate and stationary liquid phase and aqueous sodium ammonia, the distribution coefficient of sulfite tartrate as mobile phase. With use of a column increased, but that of tellurite and selenite (10.4 cm x 8.4 mm) separation was achieved 2- remained constant even up to 75%. On the in 10 min. The SeO3 content of some contrary, on the addition of ethanol to the

196 IJRPC 2016, 6(2), 192-206 Hussein M Abdel-Fattah et al. ISSN: 22312781 samples was determined, and the general they hardly affect electrophoretic resolution 2- 2- behavior of SeO3 and TeO3 was studied. and peak width. The best analytical Fung and Lau40 studied a new capillary performance characteristics were obtained electrophoresis (CE) procedure for with the MicroMist nebulizer. Detection limits simultaneous determination of ten oxoanions with this nebulizer were found to range 2- 2- 2- 2- 3- 2- -1 (CrO4 , SeO4 , MoO4 , WO4 , VO4 , SeO3 , between 6 and 58 µg L depending on the 3- 2- 2- 3- AsO4 , TeO3 , TeO4 , and AsO3 ) which were species investigated using pressure injection baseline-separated from each other and from and below 1 µg L-1 for most of the species with - the interfering UV absorbing anions (NO3 and electromigrative injection. Analysis of soil - NO2 ) commonly found in environmental water extracts showed that it was possible to carry samples. The new background electrolyte out this technique on real samples. system developed contained 5 mmol L-1 Ogra et al.42 studied the urinary tellurium potassium phosphate and 0.007 mmol L-1 metabolite in rats administered sodium octadecyltrimethyl-ammonium hydroxide, pH tellurite. In this study, the urinary Te 11.2. The optimized working conditions were metabolites (UTMs) in rats were detected by electrokinetic sampling at -5 kV for 10 s, using HPLC-ICP-MS and electrospray running voltage at -15 kV with 5 µA current, ionization (ESI)-MS. To clear UTMs and detection wavelength at 205 nm. No identification, two different chromatographic interference was observed for non-UV- mechanisms, i.e., multi-mode gel filtration and absorbing anions and UV-absorbing anions up cation exchange column, were employed. The to 20 and 10 times higher concentrations, major UTM detected after ingestion of tellurite respectively. The analysis was fast, with a was trimethyltelluronium, and no urinary sugar complete CE run within 6 min. Wide linear metabolites containing Te were detected ranges (1-2000 µg L-1), good repeatability in despite the fact that the major urinary migration time (relative standard deviation selenometabolite was a selenosugar (methyl- RSD 0.55-2.8%), satisfactory precision in peak 2-acetamido-2-deoxy-1-seleno-b-D- area (RSD 3.8-5.6%) and peak height (RSD galactopyranoside). Interestingly, the ingestion 3.9-5.3%) measurement, and detection limits of tellurite enhanced the excretion of (1-25 µg L-1) sufficiently sensitive to detect selenometabolites in urine. These results oxoanions found in environmental water suggest that Te is discretely metabolized from samples. The reliability of the CE procedure selenium (Se), an essential element belonging developed had been established by recovery to the same group, although it affects the test and parallel method determination using metabolism of Selenium in rats. Thus, the atomic absoprtion spectrophotometry for real disturbance of Se metabolism, i.e., the river water sample. induction of Se deficiency, may be one of the Optimization of the hyphenation between potential toxic effects of Te. capillary zone electrophoresis (CZE) and A simple capillary zone electrophoretic method inductively coupled plasma mass spectrometry for the determination of important oxyanions of (ICP-MS) was studied for the simultaneous selenium and tellurium and another Se- determination of metalloid species in the containing anion, selenocyanate, has been environment41. Arsenic (arsenite, arsenate, developed43. The method used direct UV monomethylarsonic acid, dimethylarsinic acid), absorption detection and allows determination selenium (selenite, selenate, of all the analytes in less than 6 min this selenomethionine, selenocystine), antimony assay has a lower detection limit compared (antimonite) and tellurium (tellurite, tellurate) with other methods involving complex species were simultaneously separated using biological matrices and with a wide linear a 75 µm i.d. fused silica capillary using either a range. The method was applied to live cultures chromate or a phosphate electrolyte. Different of two different bacteria in two different growth nebulizers were tested for introduction in the media in time course experiments following detector. A V-groove nebulizer (the Babington) the changes in metalloid-containing anion and two concentric micronebulizers (the MCN- concentrations. The results showed that this 100 and the MicroMist) were studied in order method is a useful means in determination of to improve resolution, sensitivity and these analytes in bacterial cultures. reproducibility. The optimization of CZE-ICP- Kuo and Jiang44 described an ion MS interface operating parameters is chromatography-inductively coupled plasma discussed for each nebulizer-interface mass spectrometric (IC–ICP–MS) method for combination, and special attention is given to the speciation of selenium and tellurium the position of the capillary inside the compounds namely selenite [Se(IV)], selenate nebulizer. Different nebulizer gas and liquid [Se(VI)], Se-methylselenocysteine (MeSeCys), sheath flow rates were studied in detail and selenomethione (SeMet), tellurite [Te(IV)] and

197 IJRPC 2016, 6(2), 192-206 Hussein M Abdel-Fattah et al. ISSN: 22312781 tellurate [Te(VI)]. Chromatographic separation separation conditions were established. Under is performed in gradient elution mode using the optimal conditions, the LOD obtained for 0.5 mmol L-1 ammonium citrate in 2% Te(IV) was 0.079 ng L-1, while the precision methanol (pH 3.7) and 20 mmol L-1 ammonium was 7.0% (C = 10 ng L-1, n = 7). The proposed citrate in 2% methanol (pH 8.0). The analyses method was successfully applied to the are carried out using dynamic reaction cell speciation of inorganic tellurium in seawater. (DRC) ICP-MS. The DRC conditions have also Yang et al.46 reported a method for tellurium been optimized to obtain interference free determination in soil and plant samples using measurements of 78Se+ and 80Se+ which are sector field inductively coupled plasma mass otherwise interfered by 38Ar40Ar+ and 40Ar40Ar+, spectrometry (SF-ICP-MS). Soil and plant respectively. The detection limits of the samples were digested using Aqua regia. After procedure are in the range 0.01–0.03 ng Se appropriate dilution, Te in soil and plant mL-1 and 0.01–0.08 ng Te mL-1. The accuracy samples was directly analyzed without any of the method has been verified by comparing separation and preconcentration. This sample the sum of the concentrations of individual preparation approach avoided to a maximum species obtained by the present procedure extent any contamination and loss of Te prior with the total concentration of the elements in to the analysis. The developed analytical two NIST SRMs Whole Milk Powder RM 8435 method was validated by the analysis of and Rice Flour SRM 1568a. The selenium and soil/sediment and plant reference materials. tellurium species are extracted from milk Satisfactory detection limits of 0.17 ng g−1 for powder and rice flour samples by using soil and 0.02 ng g−1 for plant samples were Protease XIV at 70 °C on a water bath for 30 achieved, which meant that this method was min. applicable to studying the soil-to-plant transfer The speciation of inorganic tellurium species in factor of Te. This method can be used for the seawater by inductively coupled plasma-MS estimation of internal radiation dose of (ICP-MS) following selective magnetic SPE radioactive tellurium due to the Fukushima (MSPE) separation was developed by Hu45. Daiichi Nuclear Power Plant accident. Within the pH range of 2-9, tellurite (Te(IV)) Determination of Co, Ni and Te in alcoholic could be quantitatively adsorbed on c- beverages by photochemical vapor generation mercapto-propyltrimethoxysilane (c-MPTMS) combined with inductively coupled plasma modified silicacoated magnetic nanoparticles mass spectrometry was described47. Volatile (MNPs), while the tellurate (Te(VI)) remained species of Co, Ni and Te were liberated from in solution. Without filtration or centrifugation, mixed formic acid and acetic acid media these tellurite-loaded MNPs could be following exposure to a UV source. Limits of separated easily from the aqueous solution by quantification are 0.5, 0.1, and 0.4 μg L−1 for simply applying external magnetic field. The Co, Ni and Te, respectively, which correspond Te(IV) adsorbed on the MNPs could be to improvements 9, 35, and 3 times more over recovered quantitatively using a solution those obtained with conventional pneumatic containing 2 mol L-1 HCl and 0.03 mol L-1 nebulization. Method accuracy was K2Cr2O7. Te(VI) was reduced to Te(IV) by L- demonstrated by comparison of the cysteine prior to the determination of total determined Co, Ni and Te concentrations with tellurium, and its assay was based on those obtained following sample digestion and subtracting Te(IV) from total tellurium. The determination using conventional solution parameters affecting the separation were nebulization for sample introduction, resulting investigated systematically and the optimal in good agreement at a 95% confidence level

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Table 3: Literature data survey on separation and chromatographic methods for tellurium determination Technique Form of Linear Conditions of Time of Type of LOD pH Ref used Te range measurement analysis samples Paper impregnated with) Ion exchange Mixture of dowex-50 and HCl, HBr, [36 Paper chrom. Te(IV) ------Acidic --- selenite and HNO , H SO , HClO as ] 3 2 4 4 tellurite mobile phase Anion- Dowex 1-X8, 100-to 200- Mixture of Exchange mesh as anion exchange [37 Te(IV) ------Alkaline --- sulfite, selenite Resins resin and NaNO or NaOH ] 3 and tellurite as eluant Ni(II)-1,10-phenanthroline Mixture of and Co(III)-ethylenediamine Isotachophoresi selenite, Te(IV) and (with leading electrolyte to [38 s ------10.0 15 min. selenate, Te(VI) form ion-pair) ] - tellurite and 0.01 M Cl + NH (leading 3 tellurate electrolyte) Reversed- N263 (a commercial C8 to phase C10 trialkylmethyl- extraction ammonium chloride) as [39 Te(IV) ------10 min --- chromatograph stationary phase ] y sodium tartrate as mobile phase Electrokinetic sampling at -5 - kV for 10 s, running voltage Capillary Te(IV) and 1-2000 1-25 µg L [40 -1 1 at -15 kV with 5 µA current, 11.2 6 min River water electrophoresis Te(VI) µg L ] and detection wavelength at 205 nm Capillary zone Fused silica capillary and electrophoresis Te(IV) and 6-58 µg L- [41 --- 1 chromate or a phosphate as ------Soil extract (CZE)-(ICP Te(VI) ] electrolyte MS) The multi-mode gel filtration (HPLC-ICP- -1 and cation exchange 6.5 and [42 Te(IV) --- 0.9 µg L --- Rats urine MS) columns and ammonium 8.0 ] acetate as eluant Fused silica capillary with 1.27- Capillary zone Te(IV) and 0.191 µg separation voltage of -25 kV Bacterial [43 127 µg -1 10.5 6 electrophoresis Te(VI) -1 mL Detection by a photodiode cultures ] mL detector at 220 nm Te(IV) and 0.01-0.08 Gradient elution mode using 3.7 and Biological [44 (IC–ICP–MS) --- -1 ≤12 Te(VI) ng L ammonium acetate 8.0 samples ] c-mercapto- Magnetic SPE propyltrimethoxysilane 0.079 ng [45 followed by Te(IV) --- -1 modified silicacoated 2.0-9.0 --- Seawater L ] (ICP-MS) magnetic nanoparticles (MNPs) Sector field inductively 0.17 ng g-1 Samples was directly coupled plasma (soil) 0.02 analyzed without any Soil and plant [46 Te --- -1 ------mass ng g separation and samples ] spectrometry (plant) preconcentration (SF-ICP-MS) Photochemical Liberated volatile Te from vapor Alcoholic [47 Te --- 0.4 µg L-1 formic acid and acetic acid ------generation with beverages ] media directed to UV source (ICP-MS)

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5. ELECTROMETRIC METHODS pulse rate of 2 mV s-1. The effect of pH on Issa and Awad48 developed a potentiometric peak potential is discussed. Detection limits procedure for determination of quadrivalent and peak potential were 0.95 µmol L-1 at pH -1 2- tellurium Te(IV). Potassium permanganate 8.3 and 4.45 µmol L at pH 4.5 for TeO4 , - 2- -1 oxidises quadrivalent tellurium in weakly 1.13 V for TeO3 , 4.5 µmol L and -1.7 V for - - alkaline solutions quantitatively at room AsO2 , and -0.88 V for VO3 . Calibration graphs 2- 2- temperature, without requiring precautions to were rectilinear. Mixtures of TeO4 -TeO3 , 2- - 2- - be taken to exclude atmospheric oxygen. This TeO4 -VO3 , and TeO4 -AsO2 in the method was applied to determine the iso- concentration range 0.95 to 50 µmol L-1 were electric point of tellurium dioxide by estimating analysed, with relative differences between the tellurium content of buffer solutions actual and measured values in the range 1 to saturated with the dioxide. The results 10%. obtained indicate that this point lies at pH 3.8. Hassan53 studied the polarographic behaviour At this pH quantitative precipitation of tellurium of selenite and tellurite. Polarograms were dioxide takes place. obtained at 25 °C for 0.5 mmol L-1 of Se(IV) The analysis of tellurite-tellurate compounds and Te(IV) (as their Na salts) in 1 mol L-1- by means of automatic amperometric and ammonium formate, acetate, tartrate, oxalate potentiometric titrations was carried out by and benzoate solution and in the presence Cornwell49. Tellurium (VI) is determined by the and absence of Triton X-100. The form of the classical Bunsen method, where the polarograms and the mechanisms of the is absorbed in an excess of potassium iodide observed reductions are discussed. Plots of and the liberated iodine is titrated diffusion current versus concentration for the automatically with sodium thiosulfate to an reduction wave of Se(IV) in all the salt amperometric end-point. After fusion with solutions at -1.7 V versus its determination. potassium pyrosulfate, total tellurium and the Similarly, the concentration plots for Te(IV) associated metal ion are determined by were straight lines in the presence of Triton X- automatic potentiometric redox and EDTA 100. In binary mixtures of Se(IV) and Te(IV), titrations, respectively. the Te(IV) could be determined in 1 mol L-1 Tellurium, as tellurite, can be determined with ammonium formate or oxalate containing a fluoride-selective electrode50 by means of an 0.014 to 0.006% of surfactant or in 1 mol L-1 indirect procedure based on precipitation of ammonium acetate, tartrate or benzoate tellurite with excess of (III), followed containing 0.004% of surfactant. The limiting by back-titration with standard fluoride. The current was measured at -1.25 V versus SCE. end-point is located by using the Gran method, The Se(IV) was determined in the presence of and the titrations are suitable for tellurite Te(IV) in acetate, tartrate and benzoate concentrations above 1 mmol L-1. solution containing 0.004% of Triton X-100, Selig51 described a potentiometric precipitation with measurement at -1.7 V. titrations of selenite, selenate, tellurite and Tellurium ISE was prepared by Zareh and tellurate. Selenite and tellurite were titrated Amin54 from a solid membrane comprising a with sodium diethyldithiocarbamate by using a mixture of HgTeO3/Hg2Cl2 (1:1) with an 2 silver selective electrode as sensor. TeO3 internal contact of Hg metal in which a Pt wire only can be determined by potentiometric was immersed. The electrode exhibited a titration with hexadecylpyridinium chloride by Nernstian response of 29 mV/decade for the using a PVC-dioctyl phthalate-coated graphite concentration range 10 µmol L-1 to 0.1 mol L-1 rod as sensor. Silver nitrate can be used to of tellurite. The working pH range was 3.5- 2- 2- 2- titrate TeO3 , SeO3 and TeO4 . In aqueous 10.5. The ISE was fairly selective to tellurite in 2- solution SeO3 could be titrated with the presence of most common ions and was 2- Pb(NO3)2, whereas SeO4 required a medium used to determine tellurite in some binary 2- 2- of 80% methanol. Neither SeO3 and SeO4 mixtures of tellurite with chlorate, chromate, 2- 2- nor TeO3 and TeO4 could be titrated borate and arsenate. The mean recovery was sequentially. Recoveries ranged from 94.74 to 98-99% and the RSD were 0.19-0.51%. 100.84% with standard deviations from 0.1 to The electrochemical behaviour of tellurium in 0.71%. 2.5 mol L-1 NaOH solution was studied for the Depending on differential pulse polarography, recovery of tellurium from alkaline leach liquor Kamal et al.52 studied a method for of cemented Te using steady state polarization determination of tellurate, tellurite, arsenite and cyclic voltammetry55. The deposition and metavanadate. Supporting electrolytes characteristics and the potential range for a from a universal buffer series (Britton- stable deposit of tellurium were also Robinson) were used, with a SCE reference investigated. The morphology of deposited Te electrode, pulse amplitude of 100 mV and in alkaline solution showed a very porous

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nature and needle like radial growth. The S acts as a chelating agent for tellurium(IV) potential range for stable electrodeposition ions by differential pulse stripping was between -0.8 V and -0.95 V (vs Hg/HgO voltammetry, is described57. Under optimised electrode), but electrowinning could be carried operational conditions, the sensor exhibited out at more negative potentials due to the linear behaviour in the range of 2.0–300 ng 2- −1 disproportionation reaction of Te2 . mL (correlation coefficient: 0.9982) with a Laboratory-scale electrowinning experiments detection limit of 0.45 ng mL−1. The results were performed under different operating indicate that the sensor is sensitive and voltages, temperatures and initial Te effective for the determination of tellurium in concentrations. The current efficiency was water samples and certified reference about 85±90% for 50% recovery and about materials. 50±60% for 90% recovery. The purity of Biver et al58 reported a method for electrodeposited Te was higher than 99.95%. determination of trace concentrations of Te(IV) Differential pulse voltammetric determination and Te(VI) in surface by differential of trace Te(IV) was performed by Khoo and Ye pulse cathodic stripping voltammetry. It is 56. Electropolymerization of 3,3- based on the proton reduction catalysed by diaminobenzidine on a gold surface gave an the absorption of Te(IV) on the mercury adherent, stable film of poly(3,3- electrode. Under optimum conditions (0.1 mol diaminobenzidine) (PDAB). This polymer film L-1 HCl), a detection limit of about 5 ng L-1 for a retained the complexational functionalities of deposition time of 300 s is achieved. Organic its monomer, demonstrating preconcentration matter does not represent a problem at low abilities for several ions, including Se(IV) and concentrations; higher concentrations are Te(IV). Continuous flow and flow injection eliminated by adsorptive purification. Tellurium methods were developed for the sensitive and occurs primarily as Te(IV) and Te(VI) in selective determination of Te(IV). The natural water. Thus, determining total Te optimized method for the continuous flow requires the reduction of Te(VI) that it is not mode had a detection limit of 5.6×10-9 mol L-1 electroactive. A number of reduction for 10 min preconcentration. Typical relative procedures have been carefully evaluated. standard deviations for six consecutive However, there is an evidence that the determinations were 1.82 and 2.56% for addition of TiCl3 to the acidified samples can Te(IV) concentrations of 1.0×10-6 and 5.0×10-8 reduce Te(VI) at trace levels to Te(IV) reliably mol L-1, respectively (10 min and quantitatively. Therefore, the procedure preconcentration). The method was applied to described allows the direct determination of the determination of Te(IV) in real samples. total Te and its redox speciation. A modified carbon paste electrode based on multi-walled carbon nanotube and Alizarin Red

Table 4: Literature data survey on different electrometric methods for determination of tellurium Technique used Form of Te Linear range LOD Measurements Conditions pH Type of samples Ref Potentiometric titration Te(IV) ------KMnO4 oxidize Te(IV) alkaline Pure solution [48] Amperometric- Te(IV) and Sodium thiosulfate, potassium Mixture of tellurite ------[49] potentiometric titrations Te(VI) pyrosulfate and EDTA tellurate 1.0 mmol L- ISEs Te(IV) --- 1 Flouride selective electrode Neutral Pure solution [50]

AgNO or sodium Potentiometric Te(IV) and 3 8.6 and ------diethyldithiocarbamate as a --- [51] argentometric titration Te(VI) 5.0 titrant Differential pulse Te(IV) and pulse amplitude (100 mV) pulse 8.5 and Tellurite-tellurate ------1 - [52] polarography Te(VI) rate (2 mV s ) 4.5 mixture Pure In presence of Triton X-100 at - Polarography Te(IV) ------solutions,Te(IV) and [53] 1.25 V Se(IV) mixture Binary mixtures of -5 -1 -6 10 -10 mol 4.0×10 HgTeO3/Hg2Cl2 (1:1) as ion tellurite with ISE Te(IV) -1 -1 3.5-10.5 [54] L mol L recognition chlorate, chromate, borate and arsenate electrodeposition potential( -0.8 alkaline leach liquor Cyclic voltammetry Te(IV) ------alkaline [55] V to -0.95 V) of cemented Te -8 -6 -9 film of poly(3,3- Differential pulse 1×10 -2×10 5.6×10 Te(IV) -1 -1 diaminobenzidine) (PDAB) on 4.0 Human urine, soil [56] voltammetric mol L mol L gold surface - multi-walled carbon nanotube Differential pulse 2.0–300 ng 0.45 ng mL Te(IV) -1 1 and Alizarin Red S acts as a --- Water samples [57] stripping voltammetry mL chelating agent proton reduction catalysed by Differential pulse Te(IV) and Up to 10 µg -1 -1 5 ng L the absorption of Te(IV) on the Acidic Surface water [58] stripping voltammetry. Te(VI) L mercury electrode

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6. BIOLOGICAL REMOVAL OF by the protonophore carbonyl cyanide-p- TELLURITE IONS tri£uoromethoxyphenyl-hydrazone (FCCP) and Cooper and Few59 studied the uptake of by the K+/H+ exchanger nigericin. Notably, the potassium tellurite by a sensitive strain of light-driven membrane potential (ΔѰ) is 127 -1 Escherichia coli. By incorporating Te into enhanced by K2TeO3 ≥200 µmol L . Further, potassium tellurite (K2TeO3), the amount of the tellurite uptake is largely insensitive to salt absorbed by a buffered suspension of a valinomycin, strongly repressed by the tellurite-sensitive strain of Escherichia coli sulfhydryl reagent N-ethylethylmaleimide could be calculated from a measure of the (NEM) and competitively inhibited by radioactivity remaining on the washed phosphate. Tellurite is transported into cells by organisms. No radioactivity was lost by a Δ pH-dependent, non-electrogenic process washing. The system responsible for tellurite which is likely to involve the phosphate uptake was unstable at low pH but did not transporter (PiT family). deteriorate greatly over several hours at pH Amoozegar et al.62 isolated 49 strains of 5.5-7.3. The uptake of tellurite by the moderately halophilic bacteria from the salty organisms increased with time, and was most environments of Iran, a Gram-positive coccus rapid at pH 5.5 and 37 °C. This uptake has the designated as strain QW6 showed high properties of an enzyme action. Growth of capacity in the removal of toxic oxyanions of Escherichia coli in a medium containing 0.05% tellurium in a wide range of culture medium glucose decreased the activity of the factors including pH (5.5-10.5), temperature organisms, while the pH of the medium was (25-45 °C), various salts including NaCl, KCl, -1 scarcely affected. Heating to 100 °C for 20 min and Na2SO4 (0.5-4 mol L ), selenooxyanions destroyed the enzymic system. The low (2-10 mmol L-1), and at different uptake then obtained corresponded to a rapid concentrations of potassium tellurite (0.5-1 combination with the cells which were mmol L-1) under aerobic condition. Phenotypic saturated at fairly low tellurite concentrations. characterization and phylogenetic analyses Enzymic method for the determination of based on 16S rDNA sequence comparisons tellurite ions in aqueous media including blood indicated that this strain was a member of the plasma or serum is described60. The method genus Salinicoccus. The maximum tellurite based on the inhibition of Zn2+ - removal was exhibited in 1.5 mol L-1 NaCl at glycerophosphocholine phosphocholine 35 °C, while the activity reduced by 53% and phospho-diesterase by tellurite ions in the 47% at 25 and 45 °C, respectively. The presence of tetramethylammonium ions. optimum pH for removal activity was shown to Assays were carried out at 20 °C in 0.1 be 7.5, with 90% and 83% reduced removal mol L-1 glycine buffer of pH 10, containing 1 or capacities at the two extreme values of 5.5 10 mmol L-1 tetramethylammonium chloride, and 10, respectively. The impact of different 20 milliunits of the enzyme and 0.15 mmol L-1 concentrations of selenooxyanions (2-10 mmol p-nitrophenylphosphocholine substrate, with L-1) on tellurite removal by strain QW6 was varying amounts of tellurite or serum. The evaluated. The ability of strain QW6 for the nitrophenol formed was measured at 410 nm. removal of tellurite in the presence of 6 mmol The inhibition effect was expressed as a L-1 selenite increased by 25%. The percentage of the control. Calibration graphs concentration of toxic potassium tellurite in the were linear when inhibition was plotted against supernatant of the bacterial culture medium log tellurite concentration for 0.25-4 µmol L-1 in decreased by 99% (from 0.5 to 0.005 mmol L- the presence of 1 mmol L-1 1) after 6 days and the color of the medium tetramethylammonium chloride or for 50-800 changed to black due to the formation of less nmol L-1 in the presence of 10 mmol L-1 toxic elemental tellurium. tetramethylammonium chloride, with a Among 148 bacterial isolates from two types of detection limit of 50 nmol mL-1 tellurite. In the polluted water, strain STG-83 showed range 0.05-4 µmol mL-1 the RSD were 4-8.1%. maximum reduction and resistance There was no interference from phosphate, ability63. Sequencing of the 16S rDNA gene of selenite, sulfite, arsenite or thiols. The method STG-83 showed that the strain is closely was used to study the removal of tellurites by related to Bacillus pumilus and morphological thiols and the rate of uptake of tellurite by and biochemical tests confirmed the result. blood. The strain was nitrate negative, but it could The uptake by light-grown cells of reduce half of tellurite in solution containing Rhodobacter capsulatus of the highly toxic 1.0 mmol L-1 concentration and completely 2- metalloid oxyanion tellurite (TeO3 ) was reduced selenite and selenate in solutions examined61. tellurite is rapidly taken up by containing 1.0 mmol L-1. Both reduction to illuminated cells in a process which is inhibited elemental form and volatilization occurred in

202 IJRPC 2016, 6(2), 192-206 Hussein M Abdel-Fattah et al. ISSN: 22312781 case of all oxyanions tested, according to 3. Clayton GD and Clayton FE. Patty’s hydride generation atomic absorption Industrial Hygiene and Toxicology. spectroscopy and proton induced X-ray John Wiley. Chichester. UK. 1981. emission analytical methods. The strain was 4. Walter EG and Taylor DE. able to tolerate remarkably high Comparison of tellurite resistance concentrations of selenite (640 mmol L-1), determinants from the IncP alpha selenate (320 mmol L-1), and tellurite (1250 plasmid RP4Ter and the IncHII mol L-1); and tolerance to tellurite increased in plasmid pHH1508a. J bacteriol. presence of selenite and selenate. 1989;171(4):2160-2165. Biochemical tests and zymogram of extracted 5. Schroeder HA, Buckman J and culture solutions on gel electrophoresis Balassa JJ. Abnormal trace elements showed that the strain was nitrate negative in man: tellurium. J Chron Dis. and therefore, nitrate did not interfere with 1967;20(3):147-161. reduction of other oxyanions. Thus, the strain 6. Coral G, Arikan B and Coral MNU. A opens up good opportunities for the preliminary study on tellurite bioremediation of polluted water in natural resistance in pseudomonas spp. environment, since nitrate usually inhibits or isolated from hospital sewage. Pol J decelerates reduction of the mentioned toxic Environ Stud. 2006;15(3):517-520. oxyanions. 7. Brown Jr RD. Selenium and tellurium. From an extreme environment, Antarctica, 123 US Geological Survey Minerals tellurite-resistant bacteria were isolated64, and Yearbook. Bureau Assoc. six new tellurite-resistant and tellurite-reducing Pennsylvania, USA. 1994;67.1-67.4 bacterial strains were characterized. These 8. Taylor A. Biochemistry of tellurium. In strains were identified according to their 16S New Perspectives in the Research of rRNA gene sequence as Staphylococcus Hardly Known Trace Elements. hameolyticus, Staphylococcus sciuri, Budapest University of Horticulture Acinetobacter haemolyticus, Pseudomonas and Food Science, Budapest, lini, and two strains of Psychrobacter Hungary. 1994;147-158. immobilis. The isolates display tellurite- 9. Ha J, Sun HW, Sun JM, Zhang DQ resistance about 35 to 500 fold higher than and Yang LL. Determination of Escherichia coli (Te-sensitive organism), and a tellurium in urine by hydride high level of tellurite reduction which might be generation atomic absorption interesting for an application in the field of spectrometry with derivative signal bioremediation or nanoparticle biosynthesis. processing. Anal Chim Acta. 2001;448:145-149. CONCLUSION 10. Steinberg HH, Massari SC, Miner AC This review describes several methods for the and Rink R. Industrial exposure to determination of tellurium in environmental tellurium: atmospheric studies and and biological samples. Despite the significant clinical evaluation. J Ind Hyg Toxicol. progress, current methods still suffer from 1942;24:183-192. sample preconcentration, inappropriate 11. Karlson U and Frankenberger WT. detection limits and lack of speciation of Metal ions in biological systems. tellurium and its acid forms in chemical Marcel Dekker, New York. 1993;185– environments. Although Te is not abundant in 227. the earth crust, it is often found with other 12. Taylor DE. Bacterial tellurite elements such as As, Sb, S and Se with resistance. Trends Microbiol. similar chemical properties. Researchers are 1999;7(3):111-115. faced with several challenges for determining 13. Moore MD and Kaplan S. Identification tellurium in the presence of chemical of intrinsic high-level resistance to interferences and real samples at low cast by rare-earth and oxyanions in easily manipulation technique. members of the class proteobacteria: characterization of tellurite, selenite, REFERENCES and sesquioxide reduction in 1. Taylor DE. Bacterial tellurite Rhodobacter sphaeroides. J bacteriol. resistance. Trends Microbiol. 1992;174(5):1505-1514. 1999;7(3): 111-115. 14. Turner RJ, Weiner JH and Taylor DE. 2. Taylor A. Biochemistry of tellurium. Tellurite-mediated thiol oxidation in Biol Trace Elem. Res. 1996;55:231- Escherichia coli. Microbiology. 239. 1999;145(9):2549-2557.

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