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Behavioral Ecology and Sociobiology

, Volume 70, Issue 5, pp 809–820 | Cite as

Oxidative stress ecology and the d-ROMs test: facts, misfacts and an appraisal of a decade’s work

  • David Costantini
Methods Paper

Abstract

In recent years, behavioural ecologists have taken to studying oxidative stress in free-ranging organisms because it has been proposed as an important mediator of life-history trade-offs. A plethora of methodological approaches to quantify biomarkers associated with oxidative stress exist, each one with its own strengths and weaknesses. The d-ROMs test has emerged as one of the favoured assays in ecological studies because of its reliability, sensitivity to specific perturbations of the organism’s oxidative balance and medical and ecological relevance. Criticisms have been, however, raised about its specificity for oxidative damage. In this article, I have reviewed basic information about the d-ROMs test, its validation, the methodological mistakes made in the studies that attempted to criticise this assay and the application of this assay to ecological studies of oxidative stress. All the direct and indirect evidences show that the d-ROMs test is a valuable assay for the quantification of plasma or serum primary (or early) oxidative damage molecules and, possibly, of other biological matrices and provides ecologically relevant information.

Keywords

Biomarker Life-history Oxidative damage Physiology 

Notes

Acknowledgments

I thank the Associate Editor, three anonymous reviewers, Angelo Alberti and Stefania Casagrande for providing valuables comments that helped me to improve the presentation of the article; Katherine Herborn for kindly providing data on Phalacrocorax aristotelis reported in Table 3. Research Foundation of Flanders has supported this work.

References

  1. Alberti A, Bolognini L, Macciantelli D, Caratelli M (2000) The radical cation of N,N-diethyl-para-phenylendiamine: a possible indicator of oxidative stress in biological samples. Res Chem Intermed 26:253–267CrossRefGoogle Scholar
  2. Al-Johany AM, Haffor AS (2009) Effects of cadmium exposure on the ultrastructural pathology of different pulmonary cells, leukocyte count, and activity of glutathione peroxidase and lactate dehydrogenase in relation to free radical production in Uromastyx aegyptius. Ultrastruct Pathol 33:39–347CrossRefPubMedGoogle Scholar
  3. Assenza G, Zappasodi F, Squitti R et al (2009) Neuronal functionality assessed by magnetoencephalography is related to oxidative stress system in acute ischemic stroke. NeuroImage 44:1267–1273CrossRefPubMedGoogle Scholar
  4. Bailey HH (1998) L-S, R-buthionine sulfoximine: historical development and clinical issues. Chem Biol Interact 111–112, 239–254Google Scholar
  5. Balkaya M, Prinz V, Custodis F et al (2011) Stress worsens endothelial function and ischemic stroke via glucocorticoids. Stroke 42:3258–3264CrossRefPubMedGoogle Scholar
  6. Banfi G, Malavazos A, Iorio EL, Dolci A, Doneda L, Verna R, Corsi MM (2006) The iron-o-dianisidine/xylenol orange assay in comparative oxidative stress assessment. Some possible shortcomings. Eur J Appl Physiol 97:506–508CrossRefGoogle Scholar
  7. Beaulieu M, Mboumba S, Willaume E, Kappeler PM, Charpentier MJ (2014) The oxidative cost of unstable social dominance. J Exp Biol 217:2629–2632CrossRefPubMedGoogle Scholar
  8. Beaulieu M, González-Acuña D, Thierry AM, Polito MJ (2015) Relationships between isotopic values and oxidative status: insights from populations of gentoo penguins. Oecologia 177:1211–1220CrossRefPubMedGoogle Scholar
  9. Bednarek J, Wysocki H, Sowinski J (2004) Oxidation products and antioxidant markers in plasma of patients with Graves’ disease and toxic multinodular goiter: effect of methimazole treatment. Free Radic Res 38:659–664CrossRefPubMedGoogle Scholar
  10. Benedetti S, Lamorgese A, Piersantelli M, Pagliarani S, Benvenuti F, Canestrari F (2004) Oxidative stress and antioxidant status in patients undergoing prolonged exposure to hyperbaric oxygen. Clin Biochem 37:312–317CrossRefPubMedGoogle Scholar
  11. Bernabucci U, Colavecchia L, Danieli PP, Basiricò L, Lacetera N, Nardone A, Ronchi B (2011) Aflatoxin B1 and fumonisin B1 affect the oxidative status of bovine peripheral blood mononuclear cells. Toxicol In Vitro 25:684–691CrossRefPubMedGoogle Scholar
  12. Bertuglia S, Giusti A (2003) Microvascular oxygenation, oxidative stress, NO suppression and superoxide dismutase during postischemic reperfusion. Am J Physiol Heart Circ Physiol 285:H1064–1071CrossRefPubMedGoogle Scholar
  13. Blount JD, Vitikainen EIK, Stott I, Cant MA (2015) Oxidative shielding and the cost of reproduction. Biol Rev (published online, doi:  10.1111/brv.12179)
  14. Boncoraglio G, Caprioli M, Saino N (2012) Solicitation displays reliably reflect oxidative damage in barn swallow nestlings. Behav Ecol Sociobiol 66:539–546CrossRefGoogle Scholar
  15. Bonisoli-Alquati A, Mousseau TA, Møller AP, Caprioli M, Saino N (2010) Increased oxidative stress in barn swallows from the Chernobyl region. Comp Biochem Physiol A 155:205–210CrossRefGoogle Scholar
  16. Brambilla G, Civitareale C, Ballerini A, Fiori M, Amadori M, Archetti LI, Regini M, Betti M (2002) Response to oxidative stress as a welfare parameter in swine. Redox Rep 7:159–163CrossRefPubMedGoogle Scholar
  17. Buonocore G, Perrone S, Longini M, Terzuoli L, Bracci R (2000) Total hydroperoxide and advanced oxidation protein products in preterm hypoxic babies. Pediatr Res 47:221–224CrossRefPubMedGoogle Scholar
  18. Cadet J, Di Mascio P (2006) Peroxides in biological system. In: Rappaport Z (ed) The chemistry of peroxides. John Wiley & Sons Ltd, Chichester, pp 915–999CrossRefGoogle Scholar
  19. Calabrese L, Carbonaro M (1986) An e.p.r. study of the non-equivalence of the copper of caeruloplasmin. Biochem J 238:291–295CrossRefPubMedPubMedCentralGoogle Scholar
  20. Casagrande S, Dell’Omo G, Costantini D, Tagliavini J, Groothuis T (2011) Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian kestrel: a multi-factorial study. Comp Biochem Physiol A 160:16–26CrossRefGoogle Scholar
  21. Casagrande S, Costantini D, Groothuis TGG (2012) Interaction between sexual steroids and immune response in affecting oxidative status of birds. Comp Biochem Physiol A 163:296–301CrossRefGoogle Scholar
  22. Casagrande S, Pinxten R, Zaid E, Eens M (2014) Carotenoids, birdsong and oxidative status: administration of dietary lutein is associated with an increase in song rate and circulating antioxidants (albumin and cholesterol) and a decrease in oxidative damage. PLoS ONE 9:e115899CrossRefPubMedPubMedCentralGoogle Scholar
  23. Castellini C, Lattaioli P, Dal Bosco A, Minelli A, Mugnai C (2003) Oxidative status and semen characteristics of rabbit buck as affected by dietary vitamin E, C and n-3 fatty acids. Reprod Nutr Dev 43:91–103CrossRefPubMedGoogle Scholar
  24. Colombini F, Carratelli M, Alberti A (2016) Oxidative stress, d-ROMs test and ceruloplasmin. Free Radical Res (published online, doi:  10.3109/10715762.2015.1136063)
  25. Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251PubMedGoogle Scholar
  26. Costantini D (2014) Oxidative stress and hormesis in evolutionary ecology and physiology: a marriage between mechanistic and evolutionary approaches. Springer, Berlin HeidelbergCrossRefGoogle Scholar
  27. Costantini D, Dell’Omo G (2006) Effects of T-cell-mediated immune response on avian oxidative stress. Comp Biochem Physiol A 145:137–142CrossRefGoogle Scholar
  28. Costantini D, Dell’Omo G (2015) Oxidative stress predicts long-term resight probability and reproductive success in the Scopoli’s shearwater (Calonectris diomedea). Conserv Physiol 3:cov024CrossRefGoogle Scholar
  29. Costantini D, Casagrande S, De Filippis S, Brambilla G, Fanfani A, Tagliavini J, Dell’Omo G (2006) Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J Comp Physiol B 176:329–337CrossRefPubMedGoogle Scholar
  30. Costantini D, Coluzza C, Fanfani A, Dell’Omo G (2007) Effects of carotenoid supplementation on colour expression, oxidative stress and body mass in rehabilitated captive adult kestrels (Falco tinnunculus). J Comp Physiol B 177:723–731CrossRefPubMedGoogle Scholar
  31. Costantini D, Fanfani A, Dell'Omo G (2008) Effects of corticosteroids on oxidative damage and circulating carotenoids in captive adult kestrels (Falco tinnunculus). J Comp Physiol B 178:829–835CrossRefPubMedGoogle Scholar
  32. Costantini D, Monaghan P, Metcalfe NB (2011) Biochemical integration of blood redox state in captive zebra finches (Taeniopygia guttata). J Exp Biol 214:1148–1152CrossRefPubMedGoogle Scholar
  33. Costantini D, Monaghan P, Metcalfe N (2012a) Early life experience primes resistance to oxidative stress. J Exp Biol 215:2820–2826Google Scholar
  34. Costantini D, Ferrari C, Pasquaretta C, Cavallone E, Carere C, von Hardenberg A, Réale D (2012b) Interplay between plasma oxidative status, cortisol and coping styles in wild alpine marmots, Marmota marmota. J Exp Biol 215:374–383Google Scholar
  35. Costantini D, Casasole G, Eens M (2014a) Does reproduction protect against oxidative stress? J Exp Biol 217:4237–4243Google Scholar
  36. Costantini D, Greives TJ, Hau M, Partecke J (2014b) Does urban life change blood oxidative status in birds? J Exp Biol 217:2994–2997Google Scholar
  37. Costantini D, Casasole G, AbdElgawad H, Asard H, Eens M (2016) Experimental evidence that oxidative stress influences reproductive decisions. Funct Ecol (published online, doi:  10.1111/1365-2435.12608)
  38. Criscuolo F, Font-Sala C, Bouillaud F, Poulin N, Trabalon M (2010) Increased ROS production: a component of the longevity equation in the male Mygalomorph, Brachypelma albopilosa. PLoS ONE 5:e13104CrossRefPubMedPubMedCentralGoogle Scholar
  39. Dotan Y, Lichtenberg D, Pinchuk I (2004) Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Progr Lipid Res 43:200–227CrossRefGoogle Scholar
  40. Dudek K, Bednarek D, Siwicki AK, Rokita E, Studziński T (2013) The effect of LPS injections on non-specific immune response in affected pigeons. Polish J Vet Sci 16:723–729Google Scholar
  41. Ehrenwald E, Chisolm GM, Fox PL (1994) Intact human ceruloplasmin oxidatively modifies low density lipoprotein. J Clin Invest 93:1493–1501CrossRefPubMedPubMedCentralGoogle Scholar
  42. Erel O (2005) A new automated colorimetric method for measuring total oxidant status. Clin Biochem 38:1103–1111CrossRefPubMedGoogle Scholar
  43. Favilli F, Marraccini P, Iantomasi T, Vincenzini MT (1997) Effect of orally administered glutathione on glutathione levels in some organs of rats: role of specific transporters. Brit J Nutr 78:293–300CrossRefPubMedGoogle Scholar
  44. Feng J, Ma WQ, Gu ZL, Wang YZ, Liu JX (2007) Effects of dietary copper (II) sulfate and copper proteinate on performance and blood indexes of copper status in growing pigs. Biol Trace Elem Res 120:171–178CrossRefPubMedGoogle Scholar
  45. Ferretti G, Bacchetti T, Principi F, Di Ludovico F, Viti B, Angeleri VA, Danni M, Provinciali L (2005) Increased levels of lipid hydroperoxides in plasma of patients with multiple sclerosis: a relationship with paraoxonase activity. Mult Scler 11:677–682CrossRefPubMedGoogle Scholar
  46. Fleming JJ, Santhosh S, Selvakumar R, Jose A, Eapen CE (2009) Usefulness of ferroxidase activity of ceruloplasmin in the diagnosis of Wilson’s disease. Indian J Clin Biochem 24:15–22CrossRefPubMedPubMedCentralGoogle Scholar
  47. Geiger S, Le Vaillant M, Lebard T, Reichert S, Stier A, Le Maho Y, Criscuolo F (2012) Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol Ecol 21:1500–1510CrossRefPubMedGoogle Scholar
  48. Gerardi G, Usberti M, Martini G, Albertini A, Sugherini L, Pompella A, Di LD (2002) Plasma total antioxidant capacity in hemodialyzed patients and its relationships to other biomarkers of oxidative stress and lipid peroxidation. Clin Chem Lab Med 40:104–110CrossRefPubMedGoogle Scholar
  49. Girotti AW (1998) Lipid hydroperoxide generation, turnover, and effector action in biological systems. J Lipid Res 39:1529–1542PubMedGoogle Scholar
  50. Goldstein IM, Kaplan B (1979) Ceruloplasmin. A scavenger of superoxide anion radicals. J Biol Chem 254:4040–4045PubMedGoogle Scholar
  51. Griffith OW, Meister A (1979) Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J Biol Chem 254:7558–7560PubMedGoogle Scholar
  52. Halliwell BH, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, OxfordGoogle Scholar
  53. Harma MI, Harma M, Erel O (2006) Measuring plasma oxidative stress biomarkers in sport medicine. Eur J Appl Physiol 97:505CrossRefPubMedGoogle Scholar
  54. Hau M, Haussmann MF, Greives TJ, Matlack C, Costantini D, Quetting M, Adelman JS, Miranda AC, Partecke J (2015) Repeated stressors in adulthood increase the rate of biological ageing. Front Zool 12:4CrossRefPubMedPubMedCentralGoogle Scholar
  55. Haussmann MF, Longenecker AS, Marchetto NM, Juliano SA, Bowden RM (2012) Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proc R Soc Lond B 279:1447–1456CrossRefGoogle Scholar
  56. Herborn KA, Coffey J, Larcombe SD, Alexander L, Arnold KE (2011) Oxidative profile varies with personality in European greenfinches. J Exp Biol 214:1732–1739CrossRefPubMedGoogle Scholar
  57. Herborn KA, Daunt F., Heidinger BJ, Granroth-Wilding HMV, Burthe SJ, Newell MA, Monaghan P (2016) Age, oxidative stress exposure and fitness in a long-lived seabird. Funct Ecol (published online, doi:  10.1111/1365-2435.12578)
  58. Hussain I, Zhang Y, Huang S (2014) Degradation of aniline with zero-valent iron as an activator of persulfate in aqueous solution. RSC Adv 4:3502CrossRefGoogle Scholar
  59. Iamele L, Fiocchi R, Vernocchi A (2002) Evaluation of an automated spectrophotometric assay for reactive oxygen metabolites in serum. Clin Chem Lab Med 40:673–676Google Scholar
  60. Isaksson C, Sepil I, Baramidze V, Sheldon BC (2013) Explaining variance of avian malaria infection in the wild: the importance of host density, habitat, individual life-history and oxidative stress. BMC Ecol 13:15CrossRefPubMedPubMedCentralGoogle Scholar
  61. Ito Y, Nakamura A, Adachi M, Kato A, Ishikawa H, Maruta K, Hata T (2009) Blood oxidative stress levels and urinary dopamine values reflect the impact of academic stress on rodents. J Anal Bio-Sci 32:422–426Google Scholar
  62. Jones DP (2006) Redefining oxidative stress. Antioxid Redox Sign 8:1865–1879CrossRefGoogle Scholar
  63. Kagan VE, Borisenko GG, Tyurina YY, Tyurin VA, Jiang J, Potapovich AI, Kini V, Amoscato AA, Fujii Y (2004) Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine. Free Radic Biol Med 37:1963CrossRefPubMedGoogle Scholar
  64. Kautz L, Jung G, Valore EV, Rivella S, Nemeth E, Ganz T (2014) Identification of erythroferrone as an erythroid regulator of iron metabolism. Nat Genet 46:678–684CrossRefPubMedPubMedCentralGoogle Scholar
  65. Kilk K, Meitern R, Härmson O, Soomets U, Hõrak P (2014) Assessment of oxidative stress in serum by d-ROMs test. Free Radic Res 48:883–889CrossRefPubMedGoogle Scholar
  66. Kotani K, Tsuzaki K, Taniguchi N, Sakane N (2013) Correlation between reactive oxygen metabolites & atherosclerotic risk factors in patients with type 2 diabetes mellitus. Indian J Med Res 137:742–748PubMedPubMedCentralGoogle Scholar
  67. Kulmacz R, Miller JJ, Pendleton R, Lands W (1990) Cyclooxigenase initiation assay for hydroperoxides. Methods Enzymol 186:431–438CrossRefPubMedGoogle Scholar
  68. Kusuma Kumari M, Sankaranarayana T (2014) Evaluation of oxidative stress in type 2 diabetes mellitus patients. IOSR J Dent Med Sci 13:46–50CrossRefGoogle Scholar
  69. Lajtha A, Tettamanti G, Goracci G (2009) Handbook of neurochemistry and molecular neurobiology, 3rd edn, Neural lipids. Springer Science, New YorkCrossRefGoogle Scholar
  70. Lee C, Yoon J (2004) Temperature dependence of hydroxyl radical formation in the hv/Fe3+/H2O2 and Fe3+/H2O2 systems. Chemosphere 56:923–934CrossRefPubMedGoogle Scholar
  71. Liang Y, Roede JR, Dikalov S, Miller NG, Dudley SC Jr, Quyyumi A, Jones DP (2012) Determination of ebselen-sensitive reactive oxygen metabolites (ebROM) in human serum based upon N,N’-diethyl-1,4-phenylenediamine oxidation. Clin Chim Acta 414:1–6CrossRefPubMedPubMedCentralGoogle Scholar
  72. Lin H, Deculypere E, Buyse J (2004) Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus)—2. Short-term effect. Comp Biochem Physiol B 139:745–751CrossRefPubMedGoogle Scholar
  73. Lubrano V, Vassalle C, L’Abbate A, Zucchelli GC (2002) A new method to evaluate oxidative stress in humans. Immuno-Anal Biol Spe 17:172–175Google Scholar
  74. Lucas LD, French SS (2012) Stress-induced tradeoffs in a free-living lizard across a variable landscape: consequences for individuals and populations. PLoS ONE 7:e49895CrossRefPubMedPubMedCentralGoogle Scholar
  75. Lumeij JT, de Bruijne JJ (1985) Blood chemistry reference values in racing pigeons (Columba livia domestica). Avian Pathol 14:401–408CrossRefPubMedGoogle Scholar
  76. Marcus JR (1956) On the theory of oxidation-reduction reactions involving electron transfer. J Chem Phys 24:966CrossRefGoogle Scholar
  77. Maykova EV, Ismagilova RK, Alimova FK, Valeeva IH, Podolskaya AA, Kravtsova OA (2013) The association study of antioxidant status and antioxidant genes polymorphisms in patients with ischemic heart disease in the Republic of Tatarstan. World Appl Sci J 27:1367–1371Google Scholar
  78. Metcalfe NB, Alonso-Alvarez C (2010) Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol 24:984–996CrossRefGoogle Scholar
  79. Miyamoto S, Ronsein GE, Prado FM et al (2007) Biological hydroperoxides and singlet molecular oxygen generation. IUCMB Life 59:322–331CrossRefPubMedGoogle Scholar
  80. Miyazawa T (1989) Determination of phospholipid hydroperoxides in human blood plasma by a chemiluminescence-HPLC assay. Free Radic Biol Med 7:209–217CrossRefPubMedGoogle Scholar
  81. Montgomery MK, Hulbert AJ, Buttemer WA (2011) The long life of birds: the rat-pigeon comparison revisited. PLoS ONE 6:e24138CrossRefPubMedPubMedCentralGoogle Scholar
  82. Montgomery MK, Buttemer WA, Hulbert AJ (2012) Does the oxidative stress theory of aging explain longevity differences in birds? II. Antioxidant systems and oxidative damage. Exp Gerontol 47:211–222CrossRefPubMedGoogle Scholar
  83. Musci G, Bellenchi GC, Calabrese L (1999) The multifunctional oxidase activity of ceruloplasmin as revealed by anion binding studies. Eur J Biochem 265:589–597CrossRefPubMedGoogle Scholar
  84. Nagatomo F, Fujino H, Kondo H, Ishihara A (2012) Oxygen concentration-dependent oxidative stress levels in rats. Oxid Med Cell Longev 2012:381763CrossRefPubMedPubMedCentralGoogle Scholar
  85. Neyens E, Baeyens J (2003) A review of classic Fenton’s peroxidation as an advanced oxidation technique. J Hazard Mater 98:33–50CrossRefPubMedGoogle Scholar
  86. Noguera JC, Lores M, Alonso-Alvarez C, Velando A (2011) Thrifty development: early-life diet restriction reduces oxidative damage during later growth. Funct Ecol 25:1144–1153CrossRefGoogle Scholar
  87. Ovrebø KK, Svardal A (2000) The effect of glutathione modulation on the concentration of homocysteine in plasma of rats. Pharmacol Toxicol 87:103–107CrossRefPubMedGoogle Scholar
  88. Ovrebø KK, Sørbye H, Svardal A, Grong K, Svanes K (1997) Glutathione and N-acetylcysteine reduce gastric mucosal blood flow in rats. Digest Dis Sci 42:1765–1774CrossRefPubMedGoogle Scholar
  89. Pasquini A, Luchetti E, Marchetti V, Cardini G, Iorio EL (2008) Analytical performances of d-ROMs test and BAP test in canine plasma. Definition of the normal range in healthy Labrador dogs. Vet Res Commun 32:137–143CrossRefPubMedGoogle Scholar
  90. Pérez-Rodríguez L, Romero-Haro AA, Sternalski A, Muriel J, Mougeot F, Gil D, Alonso-Alvarez C (2015) Measuring oxidative stress: the confounding effect of lipid concentration in measures of lipid peroxidation. Physiol Biochem Zool 88:345–351CrossRefPubMedGoogle Scholar
  91. Riedel W, Lang U, Oetjen U, Schlapp U, Shibata M (2003) Inhibition of oxygen radical formation by methylene blue, aspirin, or alpha-lipoic acid, prevents bacterial-lipopolysaccharide-induced fever. Mol Cell Biochem 247:83–94CrossRefPubMedGoogle Scholar
  92. Samokyszyn VM, Miller DM, Reif DW, Aust SD (1989) Inhibition of superoxide and ferritin-dependent lipid peroxidation by ceruloplasmin. J Biol Chem 264:21–26PubMedGoogle Scholar
  93. Saravanan G, Ponmurugan P (2013) S-allylcysteine improves streptozotocin-induced alterations of blood glucose, liver cytochrome P450 2E1, plasma antioxidant system, and adipocytes hormones in diabetic rats. Int J Endocrinol Metab 11:e10927CrossRefPubMedPubMedCentralGoogle Scholar
  94. Sato H, Takahashi T, Sumitani K, Takatsu H, Urano S (2010) Glucocorticoid generates ROS to induce oxidative injury in the hippocampus, leading to impairment of cognitive function of rats. J Clin Biochem Nutr 47:224–232CrossRefPubMedPubMedCentralGoogle Scholar
  95. Schneeberger K, Czirjak GA, Voigt CC (2013) Inflammatory challenge increases measures of oxidative stress in a free-ranging, long-lived mammal. J Exp Biol 216:4514–4519CrossRefPubMedGoogle Scholar
  96. Schneeberger K, Czirjak G, Voigt CC (2014) Frugivory is associated with low measures of plasma oxidative stress and high antioxidant concentration in free-ranging bats. Naturwissenschaften 101:285–290CrossRefPubMedGoogle Scholar
  97. Schosinsky KH, Lehmann HP, Beeler MF (1974) Measurement of ceruloplasmin from its oxidase activity in serum by use of o-dianisidine dihydrochloride. Clin Chem 20:1556–63PubMedGoogle Scholar
  98. Schöttker B, Brenner H, Jansen EH et al (2015a) Evidence for the free radical/oxidative stress theory of ageing from the CHANCES consortium: a meta-analysis of individual participant data. BMC Med 13:300Google Scholar
  99. Schöttker B, Saum KU, Jansen EH, Boffetta P, Trichopoulou A, Holleczek B, Dieffenbach AK, Brenner H (2015b) Oxidative stress markers and all-cause mortality at older age: a population-based cohort study. J Gerontol A Biol Sci Med Sci 70:518–524Google Scholar
  100. Sgorbini M, Bonelli F, Rota A, Marmorini P, Biagi G, Corazza M, Pasquini A (2015) Maternal and neonatal evaluation of derivated reactive oxygen metabolites (d-ROMs) and biological antioxidant potential in the horse. Theriogen 83:48–51CrossRefGoogle Scholar
  101. Sies H (1991) Oxidative stress: oxidants and antioxidants. London Academic Press, LondonGoogle Scholar
  102. Simpson JA, Narita S, Gieseg S, Gebicki S, Gebicki JM, Dean RT (1992) Long-lived reactive species on free-radical damaged proteins. Biochem J 282:621–624CrossRefPubMedPubMedCentralGoogle Scholar
  103. Sirak AA, Beavis AJ, Robertson FM (1991) Enhanced hydroperoxide production by peripheral blood leukocytes following exposure of murine epidermis to 12-Otetradecanoylphorbol-13-acetate. Carcinogen 12:91–95CrossRefGoogle Scholar
  104. Spolders M, Höltershinken M, Meyer U, Rehage J, Flachowsky G (2010) Assessment of reference values for copper and zinc in blood serum of first and second lactating dairy cows. Vet Med Int 2010:194656CrossRefPubMedPubMedCentralGoogle Scholar
  105. Stier A, Massemin S, Zahn S, Tissier ML, Criscuolo F (2015) Starting with a handicap: effects of asynchronous hatching on growth rate, oxidative stress and telomere dynamics in free-living great tits. Oecologia 179:999–1010CrossRefPubMedGoogle Scholar
  106. Suominen P, Punnonen K, Rajamäki A, Irjala K (1998) Serum transferrin receptor and transferrin receptor-ferritin index identify healthy subjects with subclinical iron deficits. Blood 92:2934–2939PubMedGoogle Scholar
  107. Talukder S, Kerrisk KL, Ingenhoff L, Gabai G, Garcia S, Celi P (2014) Changes in plasma oxidative stress biomarkers in dairy cows after oestrus synchronisation with controlled internal drug release (CIDR) and prostaglandinF (PGF). Anim Prod Sci 54:1490–1496Google Scholar
  108. Talukder S, Kerrisk KL, Gabai G, Fukutomi C (2015) Changes in milk oxidative stress biomarkers in lactating dairy cows with ovulatory and an-ovulatory oestrous cycles. Anim Reprod Sci 158:86–95CrossRefPubMedGoogle Scholar
  109. Tobler M, Ballen C, Healey M, Wilson M, Olsson M (2015) Oxidant trade-offs in immunity: an experimental test in a lizard. PLoS ONE 10:e0126155CrossRefPubMedPubMedCentralGoogle Scholar
  110. Tomasetti M, Strafella E, Staffolani S, Santarelli L, Neuzil J, Guerrieri R (2010) α-Tocopheryl succinate promotes selective cell death induced by vitamin K3 in combination with ascorbate. Brit J Cancer 102:1224–1234CrossRefPubMedPubMedCentralGoogle Scholar
  111. van de Crommenacker J (2011) Hard times in paradise? Oxidative status, physiology and fitness in the tropical Seychelles warbler. PhD Thesis, University of GroningenGoogle Scholar
  112. van de Crommenacker J, Komdeur J, Burke T, Richardson DS (2011a) Spatio-temporal variation in territory quality and oxidative status: a natural experiment in the Seychelles warbler (Acrocephalus sechellensis). J Anim Ecol 80:668–680Google Scholar
  113. van de Crommenacker J, Komdeur J, Richardson DS (2011b) Assessing the cost of helping: the roles of body condition and oxidative balance in the Seychelles warbler (Acrocephalus sechellensis). PLoS ONE 6:e26423Google Scholar
  114. Vassalle C, Boni C, Di Cecco P, Ndreu R, Zucchelli GC (2006) Automation and validation of a fast method for the assessment of in vivo oxidative stress levels. Clin Chem Lab Med 44:1372–1375CrossRefPubMedGoogle Scholar
  115. Wang J, Li D, Che L, Lin Y, Fang Z, Xu S, Wu D (2014) Influence of organic iron complex on sow reproductive performance and iron status of nursing pigs. Livest Sci 160:89–96CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of BiologyUniversity of AntwerpWilrijkBelgium
  2. 2.Institute of Biodiversity, Animal Health and Comparative Medicine, School of Life SciencesUniversity of GlasgowGlasgowUK

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