Environmental Science and Pollution Research

, Volume 21, Issue 4, pp 2448–2454 | Cite as

The integrated biomarker response revisited: optimization to avoid misuse

  • S. DevinEmail author
  • T. Burgeot
  • L. Giambérini
  • L. Minguez
  • S. Pain-Devin
Research Article


The growing need to evaluate the quality of aquatic ecosystems led to the development of numerous monitoring tools. Among them, the development of biomarker-based procedures, that combine precocity and relevance, is recommended. However, multi-biomarker approaches are often hard to interpret, and produce results that are not easy to integrate in the environmental policies framework. Integrative index have been developed, and one of the most used is the integrated biomarker response (IBR). However, an analysis of available literature demonstrated that the IBR suffers from a frequent misuse and a bias in its calculation. Then, we propose here a new calculation method based on both a more simple formula and a permutation procedure. Together, these improvements should rightly avoid the misuse and bias that were recorded. Additionally, a case study illustrates how the new procedure enabled to perform a reliable classification of site along a pollution gradient based on biomarker responses used in the IBR calculations.


Biomarkers Integrated Index Environmental risk assessment Pollution Water Framework Directive 



The authors thank the French INSU-EC2CO-Cytrix program for supporting this work as part of the Sydépop project. We would like to thank Carole Cossu-Leguille, François Rodius and Alain Geffard for their participation in the Sydépop project.


  1. Aarab N, Champeau O, Mora P, Daubeze M, Garrigues P, Narbonne JF (2004) Scoring approach based on fish biomarkers applied to French river monitoring. Biomarkers 9:258–270CrossRefGoogle Scholar
  2. Artigas J, Arts G, Babut M, Caracciolo AB, Charles S, Chaumot A, Combourieu B, Dahllöf I, Despréaux D, Ferrari B, Friberg N, Garric J, Geffard O, Gourlay-Francé C, Hein M, Hjorth M, Krauss M, De Lange HJ, Lahr J, Lehtonen KK, Lettieri T, Liess M, Lofts S, Mayer P, Morin S, Paschke A, Svendsen C, Usseglio-Polatera P, van den Brink N, Vindimian E, Williams R (2012) Towards a renewed research agenda in ecotoxicology. Environ Pollut 160:201–206Google Scholar
  3. Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316CrossRefGoogle Scholar
  4. Broeg K, Lehtonen KK (2006) Indices for the assessment of environmental pollution of the Baltic Sea coasts: integrated assessment of a multi-biomarker approach. Mar Pollut Bull 53:508–522CrossRefGoogle Scholar
  5. Broeg K, Westernhagen HV, Zander S, Körting W, Koehler A (2005) The “bioeffect assessment index” (BAI): a concept for the quantification of effects of marine pollution by an integrated biomarker approach. Mar Pollut Bull 50:495–503CrossRefGoogle Scholar
  6. Chèvre N, Gagné F, Blaise C (2003) Development of a biomarker-based index for assessing the ecotoxic potential of aquatic sites. Biomarkers 8:287–298CrossRefGoogle Scholar
  7. Coulaud R, Geffard O, Xuereb B, Lacaze E, Quéau H, Garric J, Charles S, Chaumot A (2011) In situ feeding assay with Gammarus fossarum (Crustacea): modelling the influence of confounding factors to improve water quality biomonitoring. Water Res 45:6417–6429CrossRefGoogle Scholar
  8. Dagnino A, Allen JI, Moore MN, Broeg K, Canesi L, Viarengo A (2007) Development of an expert system for the integration of biomarker responses in mussels into an animal health index. Biomarkers 12:155–172CrossRefGoogle Scholar
  9. Galloway TS, Brown RJ, Browne MA, Dissanayake A, Lowe D, Depledge MH, Jones MB (2006) The ECOMAN project: a novel approach to defining sustainable ecosystem function. Mar Pollut Bull 53:186–194CrossRefGoogle Scholar
  10. Hagger JA, Jones MB, Lowe D, Leonard DRP, Owen R, Galloway TS (2008) Application of biomarkers for improving risk assessments of chemicals under the water framework directive: a case study. Mar Pollut Bull 56:1111–1118CrossRefGoogle Scholar
  11. Izagirre U, Marigómez I (2009) Lysosomal enlargement and lysosomal membrane destabilisation in mussel digestive cells measured by an integrative index. Environ Pollut 157:1544–1553CrossRefGoogle Scholar
  12. Kammann U, Biselli S, Reineke N, Wosniok W, Danischewski D, Huhnerfuss H, Kinder A, Sierts-Herrmann A, Theobald N, Vahl HH, Vobach M, Westendorf J, Steinhart H (2005) Bioassay-directed fractionation of organic extracts of marine surface sediments from the North and Baltic Sea—part II: results of the biotest battery and development of a biotest index. J Soils Sediments 5:225–232CrossRefGoogle Scholar
  13. Lam PKS (2009) Use of biomarkers in environmental monitoring. Ocean Coast Manag 52:348–354CrossRefGoogle Scholar
  14. Leinio S, Lehtonen KK (2005) Seasonal variability in biomarkers in the bivalves Mytilus edulis and Macoma balthica from the northern Baltic Sea. Comp Biochem Physiol C Toxicol Pharmacol 140:408–421CrossRefGoogle Scholar
  15. Lyons BP, Thain JE, Stentiford GD, Hylland K, Davies IM, Vethaak AD (2010) Using biological effects tools to define good environmental status under the European Union Marine Strategy Framework directive. Mar Pollut Bull 60:1647–1651CrossRefGoogle Scholar
  16. Munkittrick KR, Arens CJ, Lowell RB, Kaminski GP (2009) A review of potential methods of determining critical effect size for designing environmental monitoring programs. Environ Toxicol Chem 28:1361–1371CrossRefGoogle Scholar
  17. Raftopoulou EK, Dimitriadis VK (2010) Assessment of the health status of mussels Mytilus galloprovincialis along Thermaikos Gulf (Northern Greece): an integrative biomarker approach using ecosystem health indices. Ecotoxicol Environ Saf 73:1580–1587CrossRefGoogle Scholar
  18. Sanchez W, Porcher J-M (2009) Fish biomarkers for environmental monitoring within the Water Framework Directive of the European Union. Trends Anal Chem 28:150–158CrossRefGoogle Scholar
  19. Schlenk D (1999) Necessity of defining biomarkers for use in ecological risk assessments. Mar Pollut Bull 39:48–53CrossRefGoogle Scholar
  20. Vörösmarty CJ, McIntyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P, Glidden S, Bunn SE, Sullivan CA, Liermann CR, Davies PM (2010) Global threats to human water security and river biodiversity. Nature 467:555–561CrossRefGoogle Scholar
  21. Xuereb B, Chaumot A, Mons R, Garric J, Geffard O (2009) Acetylcholinesterase activity in Gammarus fossarum (Crustacea Amphipoda): intrinsic variability, reference levels, and a reliable tool for field surveys. Aquat Toxicol 93:225–233CrossRefGoogle Scholar
  22. Yeom D-H, Adams SM (2007) Assessing effects of stress across levels of biological organization using an aquatic ecosystem health index. Ecotoxicol Environ Saf 67:286–295CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • S. Devin
    • 1
    • 3
    Email author
  • T. Burgeot
    • 2
  • L. Giambérini
    • 1
  • L. Minguez
    • 1
  • S. Pain-Devin
    • 1
  1. 1.CNRS UMR 7360, Laboratoire Interdisciplinaire des Environnements Continentaux (LIEC)Université de LorraineMetzFrance
  2. 2.IFREMER, Département Biogéochimie et Ecotoxicologie, Laboratoire d’Ecotoxicologie, IFREMER Centre de NantesNantesFrance
  3. 3.LIEC, Campus BridouxMetzFrance

Personalised recommendations