Cited by 2,238Antioxidant Activity and Oxidative StressRedox biology and oxidative stressFree Radicals and Antioxidants

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Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean?

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Halliwell, Barry, Whiteman, Matthew·2004·British Journal of Pharmacology

DOI 10.1038/sj.bjp.0705776PMC PMC1574951

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Abstract

Free radicals and other reactive species (RS) are thought to play an important role in many human diseases. Establishing their precise role requires the ability to measure them and the oxidative damage that they cause. This article first reviews what is meant by the terms free radical, RS, antioxidant, oxidative damage and oxidative stress. It then critically examines methods used to trap RS, including spin trapping and aromatic hydroxylation, with a particular emphasis on those methods applicable to human studies. Methods used to measure oxidative damage to DNA, lipids and proteins and methods used to detect RS in cell culture, especially the various fluorescent "probes" of RS, are also critically reviewed. The emphasis throughout is on the caution that is needed in applying these methods in view of possible errors and artifacts in interpreting the results.

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Hydroxyl Radical Generation in Oxygen-treated Infants
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NADPH Oxidase of Neutrophils Elevates o,o′-Dityrosine Cross-Links in Proteins and Urine during Inflammation
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Is allantoin in serum and urine a useful indicator of exercise-induced oxidative stress in humans?
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Effect of age on the profile of alkanes in normal human breath
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Loss of oxidized and chlorinated bases in DNA treated with reactive oxygen species: implications for assessment of oxidative damage in vivo
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ReviewNO Means No and Yes: Regulation of Cell Signaling by Protein Nitrosylation
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Identification of hydroxyhydroquinone in coffee as a generator of reactive oxygen species that break DNA single strands
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Decreasing levels of tumour necrosis factor α and interleukin 6 during lowering of body mass index with orlistat or placebo in obese subjects with cardiovascular risk factors
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Hydroxyl radical generation by rheumatoid blood and knee joint synovial fluid.
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Uric Acid and Ascorbic Acid Redox Ratios in Plasma and Tracheal Aspirate of Preterm Babies with Acute and Chronic Lung Disease
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Hypoxanthine, Uric Acid and Allantoin as Indicators of in Vivo Free Radical Reactions. Description of a HPLC Method and Human Brain Microdialysis Data
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Involvement of Cytochromes P-450 2E1 and 3A4 in the 5-Hydroxylation of Salicylate in Humans
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Distribution of hydroxynonenal-modified proteins in the kainate-lesioned rat hippocampus: evidence that hydroxynonenal formation precedes neuronal cell death
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DNA damage by nitrite and peroxynitrite: Protection by dietary phenols
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Nitration of endogenous para-hydroxyphenylacetic acid and the metabolism of nitrotyrosine
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Ethane: a marker of lipid peroxidation during cardiopulmonary bypass in humans
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Selective Peroxidation and Externalization of Phosphatidylserine in Normal Human Epidermal Keratinocytes During Oxidative Stress Induced by Cumene Hydroperoxide
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Nitrone spin traps and their pyrrolidine analogs in myocardial reperfusion injury : hemodynamic and ESR implications
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Implications of the generation of reactive oxygen species by photoactivated calcein for mitochondrial studies
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3-Hydroxylysine, a Potential Marker for Studying Radical-Induced Protein Oxidation
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Pitfalls in the Use of Common Luminescent Probes for Oxidative and Nitrosative Stress
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Validation of the peroxidative indicators, cis-parinaric acid and parinaroyl-phospholipids, in a model system and cultured cardiac myocytes
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Cell-mediated reduction of protein and peptide hydroperoxides to reactive free radicals
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Oxidation Products of Uric Acid and Ascorbic Acid in Preterm Infants with Chronic Lung Disease
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6‐Hydroxydopamine increases the hydroxylation and nitration of phenylalanine in vivo: implication of peroxynitrite formation
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A new pitfall in detecting biological end products of nitric oxide—nitration, nitros(yl)ation and nitrite/nitrate artefacts during freezing
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Protein Carbonyl Measurement by ELISA
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Cellular Oxidant Stress and Advanced Glycation Endproducts of Albumin: Caveats of the Dichlorofluorescein Assay*
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Teratogenic Actions of Thermally-stressed Culinary Oils in Rats
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The steady-state levels of oxidative DNA damage and of lipid peroxidation (F2-isoprostanes) are not correlated in healthy human subjects
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Comparison of two independent aromatic hydroxylation assays in combination with intracerebral microdialysis to determine hydroxyl free radicals
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Loss of 3-Nitrotyrosine on Exposure to Hypochlorous Acid: Implications for the Use of 3-Nitrotyrosine as a Bio-markerin Vivo
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Biological Markers in Alzheimer Disease
Neugroschl, J. A., & Davis, K. L. (2002) · American Journal of Geriatric Psychiatry · doi:10.1097/00019442-200211000-00005 · Cited by 37
Assay of serum allantoin in humans by gas chromatography–mass spectrometry
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Health benefits of eating chocolate?
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Reactive oxygen species are formed in cell culture media.
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Recycling of the ascorbate free radical by human erythrocyte membranes
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Urinary level of 1,N6 ‐ethenodeoxyadenosine, a marker of oxidative stress, is associated with salt excretion and ω6‐polyunsaturated fatty acid intake in postmenopausal Japanese women
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The urinary excretion of thiobarbituric acid reactive substances and malondialdehyde by normal adult males after consuming a diet containing salmon
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Development of the Nitrone‐Based Spin Trap Agent NXY‐059 to Treat Acute Ischemic Stroke
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Peroxynitrite Reacts with 8-Nitropurines to Yield 8-Oxopurines
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Hydrogen peroxide in breath condensate during a common cold
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Time Course of Free Radical Production After Primary Coronary Angioplasty for Acute Myocardial Infarction and the Effect of Vitamin C
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Application of the new EPR spin trap 1,1,3-trimethylisoindole N-oxide (TMINO) in trapping HO? and related biologically important radicals
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DNA Repair: Insights from Urinary Lesion Analysis
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Cyclobutane Thymidine Dimers are Present in Human Urine Following Sun Exposure: Quantitation Using 32P-Postlabeling and High-Performance Liquid Chromatography
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The antioxidant action of 2‐methyl‐6‐(p‐methoxyphenyl)‐3,7‐dihydroimidazo[1,2‐α]pyrazin‐3‐one (MCLA), a chemiluminescence probe to detect superoxide anions
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Evidence for Increased Oxidative Stress in Alcohol-Dependent Patients Provided by Quantification of in Vivo Salicylate Hydroxylation Products
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Urinary thymine dimers and 8‐oxo‐2′‐deoxyguanosine in psoriasis
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Aromatic Hydroxylation in Nasal Lavage Fluid Following Ambient Ozone Exposure
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Ruby Laser Irradiation (694 nm) of Human Skin Biopsies: Assessment by Electron Spin Resonance Spectroscopy of Free Radical Production and Oxidative Stress during Laser Depilation
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Photodynamic treatment and H2O2‐induced oxidative stress result in different patterns of cellular protein oxidation
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Kinetic behavior of the monodehydroascorbate radical studied by pulse radiolysis
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Spin trapping of superoxide, alkyl- and lipid-derived radicals with derivatives of the spin trap EPPN
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HPLC and LC-MS studies of hydroxylation of phenylalanine as an assay for hydroxyl radicals generated from Udenfriend’s reagent
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Synthesis and structure of 5,5-diethoxycarbonyl-1-pyrroline N-oxide (DECPO). Application to superoxide radical trapping
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Relation between natriuresis and urinary excretion of hydrogen peroxide
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In Vivo Salicylate Hydroxylation: A Potential Biomarker for Assessing Acute Ozone Exposure and Effects in Humans
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Development of a method for determination of the malondialdehyde–deoxyguanosine adduct in urine using liquid chromatography–tandem mass spectrometry
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Demonstration of the Formation of Hydroxyl Radicals in Acute Myocardial Infarction in Man Using Salicylate as Probe
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Correlative studies of urine fluorescence and free radical indicators
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Formation of 8-nitroguanine in tobacco cigarette smokers and in tobacco smoke-exposed Wistar rats
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Acute angiotensin II increases plasma F2-isoprostanes in salt-replete human hypertensives
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Mapping Oxidative DNA Damage Using Ligation-Mediated Polymerase Chain Reaction Technology
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Myeloperoxidase has Directly-opposed Effects on Nitration Reaction--Study on Myeloperoxidase-deficient Patient and Myeloperoxidase-knockout Mice
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A Validated Method for Rapid Analysis of Ethane in Breath and its Application in Kinetic Studies in Human Volunteers
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Blood Pressure Effects of Vitamin C
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Vitamin E and thetreatment and prevention of diabetes: a case for a controlled clinical trial.
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Effect of Allopurinol on Myocardial Oxygen Free Radical Production in Coronary Bypass Surgery
Tarkka, M. R. (2000) · Scandinavian Cardiovascular Journal · doi:10.1080/140174300750064549 · Cited by 17
Comparison of nitration and oxidation of tyrosine in advanced human carotid plaque proteins
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Pitfalls of using lucigenin in endothelial cells: Implications for NAD(P)H dependent superoxide formation
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Exercise training and oxidative stress in the elderly as measured by antipyrine hydroxylation products
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Biological Markers in Alzheimer Disease
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Oxidative DNA damage, antioxidants and DNA repair: applications of the comet assay
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The use of phenylalanine to detect hydroxyl radical production in vivo: a cautionary note
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Immunohistochemical Artifact for Nitrotyrosine in Eosinophils or Eosinophil Containing Tissue
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High Concentrations of Excised Oxidative DNA Lesions in Human Cerebrospinal Fluid
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Measurement of oxidative damage at individual gene levels by quantitative PCR using 8-hydroxyguanine glycosylase (OGG1)
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Coronary endothelial dysfunction is not rapidly reversible with ascorbic acid
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Products of the phospholipase A2 pathway mediate the dihydrorhodamine fluorescence response evoked by endogenous and exogenous peroxynitrite in PC12 cells
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Effects of Oxidants on Properties of Fluorescent Calcium Indicators
Sarvazyan, N. A., Swift, L., & Martı́nez–Zaguilán, R. (1998) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1997.0518 · Cited by 6
Ischaemic Preconditioning in Cardiopulmonary Bypass Surgery
Tarkka, M. R., & Wu, Z. (2000) · Scandinavian Cardiovascular Journal · doi:10.1080/713783119 · Cited by 6
[Biological markers for Alzheimer disease].
Tanaka, T., Wada, K., Yamamori, H., Tanaka, S., Kudo, T., & Takeda, M. (2003) · PubMed · Cited by 5
A highly sensitive method for the determination of protein bound 3,4-dihydroxyphenylalanine as a marker for post-translational protein hydroxylation in human tissuesex vivo
Harth, R., Gerlach, M., Riederer, P. F., & Götz, M. E. (2001) · Free Radical Research · doi:10.1080/10715760100300711 · Cited by 4
[Polyphenolic antioxidants in fruit juice. Urinary excretion and effects on biological markers for antioxidative status].
Young, J. F., Nielsen, S. E., Haraldsdóttir, J., Daneshvar, B., Lauridsen, S. T., Knuthsen, P., Crozier, A., Sandström, B., & Dragsted, L. O. (2000) · PubMed · Cited by 4
Vitamin E and the treatment and prevention of diabetes: A case for a controlled clinical trial
Halliwell, B. (2002) · National University of Singapore · Cited by 3
Self-citation
The Hydroxyl Radical Formation System in Polymorphonuclear Leukocytes.
Kawakami, N., Hayakawa, T., Shimohama, S., & Fujimoto, S. (1999) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.22.1034 · Cited by 2
Untitled work
(2000) · doi:10.1002/1531-8249(200011)48:5

Research works printed but not linked: 2

10.1042/bj3450453 · DOI
10.1172/JCI0215021 · DOI

Sorted by citations

Oxidative stress and neurodegeneration: where are we now?
Halliwell, B. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03907.x · Cited by 2,614
Self-citation
Reactive Species and Antioxidants. Redox Biology Is a Fundamental Theme of Aerobic Life
Halliwell, B. B. (2006) · PLANT PHYSIOLOGY · doi:10.1104/pp.106.077073 · Cited by 2,402
Self-citation
Fluorescence probes used for detection of reactive oxygen species
Gomes, A., Fernandes, E., & Lima, J. L. F. C. (2005) · Journal of Biochemical and Biophysical Methods · doi:10.1016/j.jbbm.2005.10.003 · Cited by 1,844
Oxidative Stress, Prooxidants, and Antioxidants: The Interplay
Rahal, A., Kumar, A., Singh, V., Yadav, B., Tiwari, R., Chakraborty, S., & Dhama, K. (2014) · BioMed Research International · doi:10.1155/2014/761264 · Cited by 1,806
Biomarkers of Oxidative Damage in Human Disease
Dalle-Donne, I., Rossi, R., Colombo, R., Giustarini, D., & Milzani, A. (2006) · Clinical Chemistry · doi:10.1373/clinchem.2005.061408 · Cited by 1,703

See all 2,238

Authors: Halliwell, B., & Whiteman, M.
Affiliations: National University of Singapore (SG)
ORCID: Halliwell, Barry
Whiteman, Matthew
Venue: British Journal of Pharmacology
Publisher: Wiley
Published: 2004-05
Volume: 142
Issue: 2
Pages: 231-255
ISSN: 0007-1188 (ISSN-L)
1476-5381
DOI: 10.1038/sj.bjp.0705776
PMC: PMC1574951
OpenAlex: W1977913875
Cited by: 2,238
References: 385
Citations by year: 2026: 47 · 2025: 51 · 2024: 77 · 2023: 78 · 2022: 92 · 2021: 103 · 2020: 127 · 2019: 106 · 2018: 110 · 2017: 113 · 2016: 123 · 2015: 129 · 2014: 134 · 2013: 141 · 2012: 134
FWCI: 6.98
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 1734 d)
Locations: British Journal of Pharmacology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
National University of Singapore (submittedVersion)
Topics: Health Sciences › Medicine › Biochemistry (medical) › Antioxidant Activity and Oxidative Stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Physical Sciences › Chemistry › Organic Chemistry › Free Radicals and Antioxidants
Keywords: reactive species, free radicals, oxidative stress, oxidative damage, antioxidants, spin trapping, aromatic hydroxylation, fluorescent probes, DNA damage, lipid peroxidation, protein oxidation, in vivo measurement, cell culture, measurement artifacts
MeSH terms: Animals, Electron Spin Resonance Spectroscopy, Humans, Predictive Value of Tests, Spectrometry, Fluorescence, Reactive Oxygen Species, Oxidative Stress, Cell Culture Techniques

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Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean?

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