Abstract
The presence of pharmaceuticals and personal care products (PPCPs) in the environment has become a real and widespread concern in recent years. Therefore, the primary goal of this study was to investigate 20 common and widely used PPCPs to assess their individual and combined effect on an important species in one trophic level, i.e., bacteria. The ecotoxicological effects of PPCPs at two different concentration ranges were determined in the bacterium Vibrio fischeri using Microtox® and were statistically analyzed using three models in the GraphPad Prism 6 program for Windows, v.6.03. A four-parameter model best fit the majority of the compounds. The half maximal effective concentration (EC50) of each PPCP was estimated using the best-fitting model and was compared with the results from a recent study. Comparative analysis indicated that most compounds showed the same level of toxicity. Moreover, the stimulatory effects of PPCPs at environmental concentrations (low doses) were assessed. These results indicated that certain compounds have traditional inverted U- or J-shaped dose–response curves, and 55 % of them presented a stimulatory effect below the zero effect-concentration point. Effective concentrations of 0 (EC0), 5 (EC5) and 50 % (EC50) were calculated for each PPCP as the ecotoxicological points. All compounds that presented narcosis as a mode of toxic action at high doses also exhibited stimulation at low concentrations. The maximum stimulatory effect of a mixture was higher than the highest stimulatory effect of each individually tested compound. Moreover, when the exposure time was increased, the hormetic effect decreased. Hormesis is being increasingly included in dose–response studies because this may have a harmful, beneficial or indifferent effect in an environment. Despite the results obtained in this research, further investigations need to be conducted to elucidate the behavior of PPCPs in aquatic environments.
Similar content being viewed by others
Abbreviations
- AI:
-
Autoinducer
- ARB:
-
Antibiotic-resistant bacteria
- ASA:
-
Acetylsalicylic acid
- DF:
-
Degree of freedom
- DLERA:
-
Detailed level ecological risk assessment
- ECF :
-
Effective concentration of PPCP that gives a bioluminescence inhibition of F percent
- ECOSAR:
-
Ecological structure activity relationship
- EC50 :
-
Half maximal effective concentration
- EPA:
-
Environmental protection agency
- K-S:
-
Kolmogorov–Smirnov distance
- LC50 :
-
Half maximal lethal concentration
- LOEC:
-
Lowest observable effect concentration
- LogKoc :
-
Logarithm of soil/water partition coefficient
- LogKow :
-
Logarithm of octanol/water partition coefficient
- m:
-
Slope of the curve
- MS:
-
Mean of square
- MSE:
-
Maximum stimulatory effect
- MSEC:
-
Maximum stimulatory effect concentration
- n:
-
Number of data
- na:
-
Not available
- NO(A)EL:
-
No observed (adverse) effect level
- NOEC:
-
No observed effect concentration
- NSAIDs:
-
Non-steroidal anti-inflammatory drugs
- NTR:
-
Normality test of residuals passed
- PCP:
-
Personal care product
- PhAC:
-
Pharmaceutical active compound
- PKa :
-
The negative logarithm of the acid dissociation constant, PCBs, Polychlorinated biphenyls
- PPCPs:
-
Pharmaceutical and personal care products
- QSARs:
-
Quantitative structure–activity relationships
- R:
-
Correlation coefficient
- S:
-
Solubility
- SD:
-
Standard deviation
- SS:
-
Sum of square
- WET:
-
Whole effluent toxicity test
- WWTP:
-
Wastewater Treatment Plant
- X:
-
Logarithm of the concentration of the PPCPs which induce the Y effect
- Y:
-
Effect on Vibrio fischeri
- YB :
-
Plateau at the left end of the curve
- YT :
-
Plateau at the right end of the curve
- ZEP:
-
Zero effect-concentration point
References
Azur Environmental (1999) MicrotoxOmni™ software for Windows® 95/98/NT. User Manual, pp 1–31
Backhaus T, Grimme LH (1999) The toxicity of antibiotic agents to the luminescent bacterium Vibrio fischeri. Chemosphere 38(14):3291–3301
Backhaus T, Porsbring T, Arrhenius Å, Brosche S, Johansson P, Blanck H (2011) Single-substance and mixture toxicity of five pharmaceuticals and personal care products to marine Periphyton communities. Environ Toxicol Chem 30(9):2030–2040. doi:10.1002/etc.586
Batt A, Kostich MS, Lazorchak JM (2008) Analysis of ecologically relevant pharmaceuticals in wastewater and surface water using selective solid-phase extraction and UPLC-MS/MS. Anal Chem 80(13):5021–5030. doi:10.1021/ac800066n
Beckon W, Parkins C, Maximovich A, Beckon AV (2008) A general approach to modeling biphasic relationships. Environ Sci Technol 42:1308–1314. doi:10.1021/es071148m
Belz RG, Cedergreen N, Sørensen H (2008) Hormesis in mixtures—can it be predicted? Sci Tot Environ 404:77–87. doi:10.1016/j.scitotenv.2008.06.008
Bouki C, Venieri D, Diamadopoulos E (2013) Detection and fate of antibiotic resistant bacteria in wastewater treatment plants: a review. Ecotoxicol Environ Saf 91:1–9
Breitholtz M, Nyholm JR, Karlsson J, Andersson PL (2008) Are individual NOEC levels safe for mixtures? A study on mixture toxicity of brominated flame–retardants in the copepod Nitocra spinipes. Chemosphere 72:1242–1249. doi:10.1016/j.chemosphere.2008.05.004
Calabrese EJ (1999) Evidence that hormesis represents an ‘‘overcompensation’’ response to a disruption in homeostasis. Ecotoxicol Environ Saf 42:135–137
Calabrese EJ (2005) Paradigm lost, paradigm found: the re-emergence of hormesis as a fundamental dose response model in the toxicological sciences. Environ Pollut 138:378–411. doi:10.1016/j.envpol.2004.10.001
Calabrese EJ (2008a) Hormesis and mixtures. Toxicol Appl Pharmacol 229:262–263. doi:10.1016/j.taap.2008.01.024
Calabrese EJ (2008b) Hormesis: why it is important to toxicology and toxicologists. Environ Toxicol Chem 27(7):1451–1474
Calabrese EJ, Baldwin LA (2000) Chemical hormesis: its historical foundations as a biological hypothesis. Hum Exp Toxicol 19:2–31
Calabrese EJ, Baldwin LA (2001) Hormesis: U-shaped dose responses and their centrality in toxicology. Trends Pharmacol Sci 22(6):285–291
Calabrese EJ, Baldwin LA (2003) HORMESIS: the dose-response revolution. Annu Rev Pharmacol Toxicol 43:175–197. doi:10.1146/annurev.pharmtox.43.100901.140223
Calabrese EJ, Blain R (2005) The occurrence of hormetic dose responses in the toxicological literature, the hormesis database: an overview. Toxicol Appl Pharm 202:289–301. doi:10.1016/j.taap.2004.06.023
Cedergreen N, Ritz C, Streibig JC (2005) Improved empirical models describing hormesis. Environ Toxicol Chem 24(12):3166–3172
Chapman PM (2002) Ecological risk assessment (ERA) and hormesis. Sci Tot Environ 288:131–140
Choi K, Meier PG (2001) Toxicity evaluation of metal plating wastewater employing the Microtox® Assay: a comparison with cladocerans and fish. Environ Toxicol 16(2):136–141. doi:10.1002/tox.1017
Christofi N, Hoffmann C, Tosh L (2002) Hormesis responses of free and immobilized light-emitting bacteria. Ecotoxicol Environ Saf 52:227–223. doi:10.1006/eesa.2002.2203. http://wwalibrary.com
Cleuvers M (2003) Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicol Let 142:185–194. doi:10.1016/S0378-4274(03)00068-7
Cleuvers M (2004) Mixture toxicity of the anti-inflammatory drugs diclofenac, ibuprofen, naproxen, and acetylsalicylic acid. Ecotoxicol Environ Saf 59:309–315. doi:10.1016/S0147-6513(03)00141-6
Conolly RB, Lutz WK (2004) Nonmonotonic dose-response relationships: mechanistic basis, kinetic modeling, and implications for risk assessment. Toxicol Sci 77:151–157. doi:10.1093/toxsci/kfh007
Daughton CG (2004) Non-regulated water contaminants: emerging research. Environ Impact Assess Rev 24:711–732
Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Persp 107(6):907–938
Deng Z, Lin Z, Zou X, Yao Z, Tian D, Wang D, Yin D (2012) Model of hormesis and its toxicity mechanism based on quorum sensing: a case study on the toxicity of sulfonamides to Photobacterium phosphoreum. Environ Sci Technol 46:7746–7754. doi:10.1021/es203490f
Dévier MH, Mazellier P, Aït-Aïssa S, Budzinski H (2011) New challenges in environmental analytical chemistry: identification of toxic compounds in complex mixtures. C R Chim 14:766–779. doi:10.1016/j.crci.2011.04.006
EPA (2009) Estimation programs interface suite TM for Microsoft® Windows, v 4.00. United States Environmental Protection Agency, Washington
Escher BI, Bramaz N, Eggen RIL, Richter M (2005) In vitro assessment of modes of toxic action of pharmaceuticals in aquatic life. Environ Sci Technol 39(9):3090–3100. doi:10.1021/es048590e
Fent K, Weston AA, Caminada D (2006) Review ecotoxicology of human pharmaceuticals. Aquat Toxicol 76:122–159. doi:10.1016/j.aquatox.2005.09.009
Fernández-Piñas F, Rodea-Palomares I, Leganés F, González-Pleiter M, Muñoz-Martín MA (2014) Evaluation of the ecotoxicity of pollutants with bioluminescent microorganism. In: Touand G, Marks R (eds) Bioluminescence: fundamentals and applications in biotechnology—volume 2, advances in biochemical engineering/biotechnology 145, Springer, Berlin Heidelberg. doi:10.1007/978-3-662-43619-6_3
Ge H-L, Liu S-S, Zhu X-W, Liu H-L, Wang L-J (2011) Predicting hormetic effects of ionic liquid mixtures on luciferase activity using the concentration addition model. Environ Sci Technol 45:1623–1629. doi:10.1021/es1018948
González-Mariño I, Quintana JB, Rodríguez I, Schrader S, Moeder M (2011) Fully automated determination of parabens, triclosan and methyl triclosan in wastewater by microextraction by packed sorbents and gas chromatography–mass spectrometry. Anal Chim Acta 684:59–66. doi:10.1016/j.aca.2010.10.049
Hereber T (2002) Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol Lett 131:5–17. doi:10.1016/S0378-4274(02)00041-3
ISO (2007) Water quality—determination of the inhibitory effect of water samples on the light emission of Vibrio fischeri (luminescent bacteria test)—Part 3: method using freeze-dried bacteria. ISO 11348–3:2007
Kefford BJ, Zalizniak L, Warne M, Nugegoda D (2008) Is the integration of hormesis and essentiality into ecotoxicology now opening Pandora’s Box? Environ Pollut 151:516–523. doi:10.1016/j.envpol.2007.04.019
Kortenkamp A, Backhaus T, Faust M (2009) State of the art report on mixture toxicity. Report for Directorate General for the Environment of the European Commission. European Commission, Luxembourg
Kot-Wasik A, Dȩbska J, Wasik A, Namieśnik J (2006) Determination of non-steroidal anti-inflammatory drugs in natural waters using off-line and on-line SPE followed by LC Coupled with DAD-MS. Chromatographia 64(1–2):13–21. doi:10.1365/s10337-006-0797-7
Kot-Wasik A, Dȩbska J, Wasik A, Namieśnik J (2007) Analytical techniques in studies of the environmental fate of pharmaceuticals and personal-care products. Trends Anal Chem 26(6):557–568. doi:10.1016/j.trac.2006.11.004
Kümmerer K (2009) The presence of pharmaceuticals in the environment due to human use—present knowledge and future challenges. J Environ Manag 90:2354–2366. doi:10.1016/j.jenvman.2009.01.023
Liu S-S, Song X-Q, Liu H-L, Zhang Y-H, Zhang J (2009) Combined photobacterium toxicity of herbicide mixtures containing one insecticide. Chemosphere 75:381–388. doi:10.1016/j.chemosphere.2008.12.026
Ma XY, Wang XC, Ngo HH, Guo W (2012) Application of Vibrio qinghaiensis sp. Q67 for ecotoxic assessment of environmental waters—a mini review. J Water Sustain 2(4):209–220. doi:10.11912/jws.2.4.209-220
Mattson MP (2008) Hormesis defined. Ageing Res Rev 7:1–7. doi:10.1016/j.arr.2007.08.007
Milton DL (2006) Quorum sensing in vibrios: complexity for diversification. Int J Med Microbiol 296:61–71. doi:10.1016/j.ijmm.2006.01.044
Ortiz de García S, Pinto GP, García-Encina PA, Irusta RI (2013) Ranking of concern, based on environmental indexes, for pharmaceutical and personal care products: an application to the Spanish case. J Environ Manag 129:384–397. doi:10.1016/j.jenvman.2013.06.035
Ortiz de García S, Pinto Pinto G, García-Encina P, Irusta-Mata R (2014) Ecotoxicity and environmental risk assessment of pharmaceuticals and personal care products in aquatic environments and wastewater treatment plants. Ecotoxicology 23(8):1517–1533. doi:10.1007/s10646-014-1293-8
OSPAR Commission (2007) Practical guidance document on whole effluent assessment. hazardous substances series. Publication Number: 316/2007. ISBN 978-1-905859-55-9. http://www.ospar.org/documents/dbase/publications/p00316/p00316_wea%20guidance%20document.pdf. Accessed 11 Mar 2014
Parvez S, Venkataraman C, Mukherji S (2006) A review on advantages of implementing luminescence inhibition test (Vibrio fischeri) for acute toxicity prediction of chemicals. Environ Int 32:265–268. doi:10.1016/j.envint.2005.08.022
Parvez S, Venkataraman C, Mukherji S (2008) Toxicity assessment of organic contaminants: evaluation of mixture effects in model industrial mixtures using 2n full factorial design. Chemosphere 73:1049–1055. doi:10.1016/j.chemosphere.2008.07.078
Parvez S, Venkataraman C, Mukherji S (2009) Nature and prevalence of non-additive toxic effects in industrially relevant mixtures of organic chemicals. Chemosphere 75:1429–1439. doi:10.1016/j.chemosphere.2009.03.005
Qin L-T, Liu S-S, Liu H-L, Zhang Y-H (2010) Support vector regression and least squares support vector regression for hormetic dose-response curves fitting. Chemosphere 78:327–334. doi:10.1016/j.chemosphere.2009.10.029
Ruby EG, Lee K-H (1998) The Vibrio fischeri-Euprymna scolopes light organ association: current ecological paradigms. Appl Environ Microbiol 64(3):805–812
Santos LHMLM, Araujo AN, Fachini A, Pena A, Delerue-Matos C, Montenegro MCBSM (2010) Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J Hazard Mat 175:45–95. doi:10.1016/j.jhazmat.2009.10.100
Shen K, Shen C, Lu Y, Tang X, Zhang C, Chen X, Shi J, Lin Q, Chen Y (2009) Hormesis response of marine and freshwater luminescent bacteria to metal exposure. Biol Res 42:183–187
Silva E, Rajapakse N, Kortenkamp A (2002) Something from “Nothing” – Eight weak estrogenic chemicals combined at concentrations below NOECs produce significant mixture effects. Environ Sci Technol 36(8):1751–1756. doi:10.1021/es0101227
SRC PhysProp Database (2014) http://www.srcinc.com/what-we-do/environmental/scientific-databases.html. Accessed 27 Mar 2014
Stebbing ARD (1998) A theory for growth hormesis. Mutation Research 403:249–258. PII: S0027- 5107(98)00014-1
Stebbing ARD (2000) Hormesis: interpreting the β-curve using control theory. J Appl Toxicol 20:93–101
Teeguarden JG, Dragan Y, Pitot HC (2000) Hazard assessment of chemical carcinogens: the impact of hormesis. J Appl Toxicol 20:113–120. doi:10.1002/(SICI)1099-1263(200003/04)20:2<113
Ternes T, Bonerz M, Schmidt T (2001) Determination of neutral pharmaceuticals in wastewater and rivers by liquid chromatography–electrospray tandem mass spectrometry. J Chromatogr A 938:175–185
United Nations (2011) Globally harmonized system of classification and labelling of chemicals (GHS), 4th edn. United Nations Publications, New York
van der Grinten E, Pikkemaat MG, van den Brandhof EJ, Stroomberg GJ, Kraak MHS (2010) Comparing the sensitivity of algal, cyanobacterial and bacterial bioassays to different groups of antibiotics. Chemosphere 80:1–6. doi:10.1016/j.chemosphere.2010.04.011
Vighi M, Migliorati S, Monti GS (2009) Toxicity on the luminescent bacterium Vibrio fischeri (Beijerinck). I: QSAR equation for narcotics and polar narcotics. Ecotoxicol Environ Saf 72:154–161. doi:10.1016/j.ecoenv.2008.05.008
Villa S, Migliorati S, Monti GS, Vighi M (2012) Toxicity on the luminescent bacterium Vibrio fischeri (Beijerinck). II: response to complex mixtures of heterogeneous chemicals at low levels of individual components. Ecotoxicol Environ Saf 86:93–100. doi:10.1016/j.ecoenv.2012.08.030
Warne MSJ, van Dam R (2008) NOEC and LOEC should no longer be generated or used. Australas J Ecotoxicol 14:1–5
Zhang J, Liu S-S, Dou R-N, Liu H-L, Zhang J (2011) Evaluation on the toxicity of ionic liquid mixture with antagonism and synergism to Vibrio qinghaiensis sp.-Q67. Wat Res 47:833–840. doi:10.1016/j.chemosphere.2010.10.063
Zhang J, Liu S-S, Yu Z-Y, Zhang J (2013a) Time-dependent hormetic effects of 1-alkyl-3-methylimidazolium bromide on Vibrio qinghaiensis sp.-Q67: luminescence, redox reactants and antioxidases. Chemosphere 91:462–467
Zhang J, Liu S-S, Yu Z-Y, Liu H-L, Zhang J (2013b) The time-dependent hormetic effects of 1-alkyl-3-methylimidazolium chloride and their mixtures on Vibrio qinghaiensis sp. -Q67. J Hazard Mat 258–259:70–76. doi:10.1016/j.jhazmat.2013.02.057
Zou X, Lin Z, Deng Z, Yin D (2013) Novel approach to predicting hormetic effects of antibiotic mixtures on Vibrio fischeri. Chemosphere 90:2070–2076
Acknowledgments
The authors would like to thank the Environmental Technology Group of the University of Valladolid for supporting this research and Carabobo University, Venezuela for the Ph.D. scholarship Grants (Nos. CD-3417 and CD-2155).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de García, S.O., García-Encina, P.A. & Irusta-Mata, R. Dose–response behavior of the bacterium Vibrio fischeri exposed to pharmaceuticals and personal care products. Ecotoxicology 25, 141–162 (2016). https://doi.org/10.1007/s10646-015-1576-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-015-1576-8