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Brodin, Tomas
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Publications (10 of 68) Show all publications
Sundin, J., Jutfelt, F., Thorlacius, M., Fick, J. & Brodin, T. (2019). Behavioural alterations induced by the anxiolytic pollutant oxazepam are reversible after depuration in a freshwater fish. Science of the Total Environment, 665, 390-399
Open this publication in new window or tab >>Behavioural alterations induced by the anxiolytic pollutant oxazepam are reversible after depuration in a freshwater fish
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2019 (English)In: Science of the Total Environment, ISSN 0048-9697, E-ISSN 1879-1026, Vol. 665, p. 390-399Article in journal (Refereed) Published
Abstract [en]

Anthropogenic pharmaceutical pollutants have been detected in nature across the globe, and recent work has shown negative effects of pharmaceuticals on the health and welfare of many animals. However, whether alterations can be reversed has been poorly investigated, although such studies are essential to assess the effects of high-peak exposure events in waterways where pharmaceutical concentrations are usually low. In this study, we investigated the effects of two concentrations (environmentally relevant 1 μg L−1 and high 100 μg L−1) of oxazepam, an anxiolytic commonly detected in aquatic environments, and whether behavioural alterations are reversible after depuration. Specifically, we measured daytime and night-time swimming activity and daytime behaviours related to boldness (foraging, sheltering and routine swimming activity) using the freshwater burbot (Lota lota). We found that both swimming activity and boldness were affected by oxazepam. Fish exposed to the higher level had a higher burst swimming duration (i.e., fast swimming bouts), both in the daytime and night-time trials. Further, fish exposed to the lower oxazepam level spent less time sheltering than control- and high-level exposed fish, but there was no difference between the control and high oxazepam treatments. For routine swimming activity, quantified in the boldness trials, and for latency to forage, there were no treatment effects. When retesting the fish after depuration, the detected behavioural alterations were no longer present. Since the magnitude of these effects were not consistent across endpoints, our study suggests that oxazepam might not be a great concern for this particular, stress tolerant, species, highlighting the importance of evaluating species-specific effects of pharmaceuticals. The observation that the effects we did find were reversible after depuration is encouraging, and indicates that rapid restoration of behaviours after removal from oxazepam contamination is possible.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Benzodiazepines, Boldness, Swimming activity, Pharmaceutical contaminants
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-157731 (URN)10.1016/j.scitotenv.2019.02.049 (DOI)000460628600040 ()30772569 (PubMedID)2-s2.0-85061438548 (Scopus ID)
Available from: 2019-04-10 Created: 2019-04-10 Last updated: 2019-04-10Bibliographically approved
Saaristo, M., Lagesson, A., Bertram, M. G., Fick, J., Klaminder, J., Johnstone, C. P., . . . Brodin, T. (2019). Behavioural effects of psychoactive pharmaceutical exposure on European perch (Perca fluviatilis) in a multi-stressor environment. Science of the Total Environment, 655, 1311-1320
Open this publication in new window or tab >>Behavioural effects of psychoactive pharmaceutical exposure on European perch (Perca fluviatilis) in a multi-stressor environment
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2019 (English)In: Science of the Total Environment, ISSN 0048-9697, E-ISSN 1879-1026, Vol. 655, p. 1311-1320Article in journal (Refereed) Published
Abstract [en]

With the ability to resist biodegradation and exert therapeutic effects at low concentrations, pharmaceutical contaminants have become environmental stressors for wildlife. One such contaminant is the anxiolytic oxazepam, a psychoactive pharmaceutical that is frequently detected in surface waters globally. Despite growing interest in understanding how wildlife respond to anxiolytics, synergistic effects of pharmaceuticals and other abiotic (e.g. temperature) and biotic (e.g. predation risk) stressors remain unclear. Here, using a multi-stressor approach, we investigated effects of 7-day oxazepam exposure (6.5 μg/L) on anxiety-related behaviours in juvenile European perch (Perca fluviatilis). The multi-stressor approach was achieved by exposing perch to oxazepam at two temperatures (10 °C and 18 °C), and at two predation risk regimes—generated using chemical cues from the northern pike (Esox lucius). Our exposures resulted in a successful uptake of the drug from the water, i.e., oxazepam was measured in perch muscle tissue at 50 ± 17 ng/g (mean ± SD). We found significant oxazepam-induced effects on boldness, with 76.7% of the treated fish entering the white background (i.e. ‘exposed’ area where exposure to presumed risks are higher) within the first 5 min, compared to 66.6% of the control fish. We also found a significant effect of temperature on total time spent freezing (i.e. staying motionless). Specifically, fish in the low temperature treatments (oxazepam, predation) froze for longer than fish in high temperatures. Our multi-stressor study is the first to uncover how anxiety-related behaviours in wild juvenile fish are altered by changes in water temperature and perceived predation risk. Importantly, our findings highlight the need to focus on multiple stressors to improve understanding of how organisms not only survive, but adapt to, human-induced environmental change.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Anti-predator behaviour, Behavioural ecotoxicology, Oxazepam, Pharmaceuticals, Temperature effect
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-155752 (URN)10.1016/j.scitotenv.2018.11.228 (DOI)000455034600127 ()30577123 (PubMedID)
Funder
Swedish Research Council Formas, 2013-4431
Available from: 2019-01-28 Created: 2019-01-28 Last updated: 2019-01-28Bibliographically approved
Jonsson, M., Andersson, M., Fick, J., Brodin, T., Klaminder, J. & Piovano, S. (2019). High-speed imaging reveals how antihistamine exposure affects escape behaviours in aquatic insect prey. Science of the Total Environment, 648, 1257-1262
Open this publication in new window or tab >>High-speed imaging reveals how antihistamine exposure affects escape behaviours in aquatic insect prey
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2019 (English)In: Science of the Total Environment, ISSN 0048-9697, E-ISSN 1879-1026, Vol. 648, p. 1257-1262Article in journal (Refereed) Published
Abstract [en]

Aquatic systems receive a wide range of pharmaceuticals that may have adverse impacts on aquatic wildlife. Among these pharmaceuticals, antihistamines are commonly found, and these substances have the potential to influence the physiology of aquatic invertebrates. Previous studies have focused on how antihistamines may affect behaviours of aquatic invertebrates, but these studies probably do not capture the full consequences of antihistamine exposure, as traditional recording techniques do not capture important animal movements occurring at the scale of milliseconds, such as prey escape responses. In this study, we investigated if antihistamine exposure can impact escape responses in aquatic insect, by exposing damselfly (Coenagrion hastulatum) larvae to two environmentally relevant concentrations (0.1 and 1 μg L−1) of diphenhydramine. Importantly, we used a high-speed imaging approach that with high-time resolution captures details of escape responses and, thus, potential impacts of diphenhydramine on these behaviours. Our results show overall weak effects of antihistamine exposure on the escape behaviours of damselfly larvae. However, at stage 2 of the C-escape response, we found a significant increase in turning angle, which corresponds to a reduced swimming velocity, indicating a reduced success at evading a predator attack. Thus, we show that low concentrations of an antihistamine may affect behaviours strongly related to fitness of aquatic insect prey – effects would have been overlooked using traditional recording techniques. Hence, to understand the full consequences of pharmaceutical contamination on aquatic wildlife, high-speed imaging should be incorporated into future environmental risk assessments.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Damselfly larvae, Diphenhydramine, Escape response, Pharmaceutical pollution
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-150912 (URN)10.1016/j.scitotenv.2018.08.226 (DOI)2-s2.0-85052146409 (Scopus ID)
Available from: 2018-08-20 Created: 2018-08-20 Last updated: 2018-11-12Bibliographically approved
McCallum, E., Sundelin, A., Fick, J., Alanärä, A., Klaminder, J., Hellström, G. & Brodin, T. (2019). Investigating tissue bioconcentration and the behavioural effects of two pharmaceutical pollutants on sea trout (Salmo trutta) in the laboratory and field. Aquatic Toxicology, 207, 170-178
Open this publication in new window or tab >>Investigating tissue bioconcentration and the behavioural effects of two pharmaceutical pollutants on sea trout (Salmo trutta) in the laboratory and field
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2019 (English)In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 207, p. 170-178Article in journal (Refereed) Published
Abstract [en]

Pharmaceuticals entering aquatic ecosystems via wastewater effluents are of increasing concern for wild animals. Because some pharmaceuticals are designed to modulate human behaviour, measuring the impacts of exposure to pharmaceuticals on fish behaviour has become a valuable endpoint. While laboratory studies have shown that pharmaceuticals can affect fish behaviour, there is a lack of understanding if behaviour is similarly affected in natural environments. Here, we exposed sea trout (Salmo trutta) smolts to two concentrations of two pharmaceutical pollutants often detected in surface waters: temazepam (a benzodiazepine, anxiolytic) or irbesartan (an angiotensin II receptor blocker, anti-hypertensive). We tested the hypothesis that changes to behavioural traits (anxiety and activity) measured in laboratory trials following exposure are predictive of behaviour in the natural environment (downstream migration). Measures of anxiety and activity in the laboratory assay did not vary with temazepam treatment, but temazepam-exposed fish began migrating faster in the field. Activity in the laboratory assay did predict overall migration speed in the field. In contrast to temazepam, we found that irbesartan exposure did not affect behaviour in the laboratory, field, or the relationship between the two end-points. However, irbesartan was also not readily taken up into fish tissue (i.e. below detection levels in the muscle tissue), while temazepam bioconcentrated (bioconcentration factor 7.68) rapidly (t(1/2) < 24 h). Our findings add to a growing literature showing that benzodiazepine pollutants can modulate fish behaviour and that laboratory assays may be less sensitive at detecting the effects of pollutants compared to measuring effects in natural settings. Therefore, we underscore the importance of measuring behavioural effects in the natural environment.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Ecotoxicology, Scototaxis, Steady-state, In situ, Bioconcentration
National Category
Oceanography, Hydrology and Water Resources Ecology Pharmacology and Toxicology
Identifiers
urn:nbn:se:umu:diva-162518 (URN)10.1016/j.aquatox.2018.11.028 (DOI)000457659300019 ()30576864 (PubMedID)
Available from: 2019-08-21 Created: 2019-08-21 Last updated: 2019-08-21Bibliographically approved
McCallum, E. S., Lindberg, R. H., Andersson, P. L. & Brodin, T. (2019). Stability and uptake of methylphenidate and ritalinic acid in nine-spine stickleback (Pungitius pungitius) and water louse (Asellus aquaticus). Environmental science and pollution research international, 26(9), 9371-9378
Open this publication in new window or tab >>Stability and uptake of methylphenidate and ritalinic acid in nine-spine stickleback (Pungitius pungitius) and water louse (Asellus aquaticus)
2019 (English)In: Environmental science and pollution research international, ISSN 0944-1344, E-ISSN 1614-7499, Vol. 26, no 9, p. 9371-9378Article in journal (Refereed) Published
Abstract [en]

The presence of human pharmaceuticals in the environment has garnered significant research attention because these compounds may exert therapeutic effects on exposed wildlife. Yet, for many compounds, there is still little research documenting their stability in the water column and uptake in organism tissues. Here, we measured the uptake and stability of methylphenidate (Ritalin (R), a frequently prescribed central nervous system stimulant) and its primary metabolite, ritalinic acid, in (1) water only or (2) with nine-spine stickleback and water louse. Methylphenidate degraded to ritalinic acid in both studies faster at a higher temperature (20 degrees C versus 10 degrees C), with concentrations of ritalinic acid surpassing methylphenidate after 48-100 h, depending on temperature. The concentration of methylphenidate in stickleback was highest at the first sampling point (60 min), while the concentration in water louse tissues reached comparatively higher levels and peaked after similar to 6 days. Neither stickleback nor water louse took up ritalinic acid in tissues despite being present in the water column. Our findings provide valuable data for use in future risk assessment of methylphenidate and will aid in the design of studies aimed at measuring any ecotoxicological effects on, for example, the behaviour or physiology of aquatic organisms.

Place, publisher, year, edition, pages
Springer, 2019
Keywords
Pharmaceuticals, Ecotoxicology, Stimulant, Behaviour, Methylphenidate, Aquatic organisms
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-158603 (URN)10.1007/s11356-019-04557-9 (DOI)000464851100088 ()30805842 (PubMedID)
Available from: 2019-05-08 Created: 2019-05-08 Last updated: 2019-05-08Bibliographically approved
Richmond, E. K., Rosi, E. J., Walters, D. M., Fick, J., Hamilton, S. K., Brodin, T., . . . Grace, M. R. (2018). A diverse suite of pharmaceuticals contaminates stream and riparian food webs. Nature Communications, 9, Article ID 4491.
Open this publication in new window or tab >>A diverse suite of pharmaceuticals contaminates stream and riparian food webs
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2018 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 9, article id 4491Article in journal (Refereed) Published
Abstract [en]

A multitude of biologically active pharmaceuticals contaminate surface waters globally, yet their presence in aquatic food webs remain largely unknown. Here, we show that over 60 pharmaceutical compounds can be detected in aquatic invertebrates and riparian spiders in six streams near Melbourne, Australia. Similar concentrations in aquatic invertebrate larvae and riparian predators suggest direct trophic transfer via emerging adult insects to riparian predators that consume them. As representative vertebrate predators feeding on aquatic invertebrates, platypus and brown trout could consume some drug classes such as antidepressants at as much as one-half of a recommended therapeutic dose for humans based on their estimated prey consumption rates, yet the consequences for fish and wildlife of this chronic exposure are unknown. Overall, this work highlights the potential exposure of aquatic and riparian biota to a diverse array of pharmaceuticals, resulting in exposures to some drugs that are comparable to human dosages.

Place, publisher, year, edition, pages
Nature Publishing Group, 2018
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-153544 (URN)10.1038/s41467-018-06822-w (DOI)000449270300001 ()30401828 (PubMedID)
Available from: 2018-11-26 Created: 2018-11-26 Last updated: 2018-11-26Bibliographically approved
Saaristo, M., Lagesson, A., Bertram, M. G., Fick, J., Klaminder, J., Johnstone, C. P., . . . Brodin, T. (2018). Behavioural effects of temperature, predation-risk and anxiolytic exposure on the European perch (Perca fluviatilis).
Open this publication in new window or tab >>Behavioural effects of temperature, predation-risk and anxiolytic exposure on the European perch (Perca fluviatilis)
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2018 (English)Manuscript (preprint) (Other academic)
Abstract [en]

With the ability to resist biodegradation and exert therapeutic effects at low concentrations, emerging contaminants have become environmental stressors for wildlife. One such contaminant is the anxiolytic oxazepam, a psychoactive pharmaceutical which is frequently detected in surface waters globally. Despite the growing interest in understanding how wildlife responds to such contaminants, the synergistic fitness effects of pharmaceuticals and increased variability in temperature remain unclear. Here, by using a multi-stressor approach, we investigated the effects of 7-d oxazepam exposure (6.5 μg/L) on anxiety-related behaviours in juvenile European perch (Perca fluviatilis). The multi-stressor approach was achieved by exposing perch to oxazepam at either low (10°C) or high (18°C) temperature, with or without a predation cue, generating 8 treatments. Our exposures resulted in a successful uptake of the drug from the water, i.e. oxazepam was measured at muscle tissue concentrations around 50 ± 17 ng/g (mean ± SD). We found significant effects on boldness induced by the studied drug: 92.8% of the fish in the 'oxazepam and predation and high temperature' treatment entered the white background (representing a novel area where exposure to presumed risks are higher) within the first 5 min, compared to 79.3% of the 'control and predation and high temperature' fish. We also found a significant effect on temperature on the total time freezing (i.e. staying motionless). Specifically, fish in the low temperature treatments (oxazepam, predation and control) froze for longer than fish in the high temperatures, respectively. Our study is the first to show altered anxiety-related behaviours in a native juvenile fish resulting from oxazepam, predation and high temperature. As adaptation to a range of biotic and abiotic pressures is essential to living organisms, our study highlights the need to focus on multiple stressors to improve understanding of how organisms not only survive, but adapt to human-induced environmental change.

Keywords
Behavioural ecotoxicology, Benzodiazepines, Freshwater fish, Multiple stressors, Scototaxis
National Category
Environmental Sciences
Research subject
Ecotoxicology
Identifiers
urn:nbn:se:umu:diva-151126 (URN)
Available from: 2018-08-28 Created: 2018-08-28 Last updated: 2018-08-28
Wang, H., Sikora, P., Rutgersson, C., Lindh, M., Brodin, T., Björlenius, B., . . . Norder, H. (2018). Differential removal of human pathogenic viruses from sewage by conventional and ozone treatments. International journal of hygiene and environmental health (Print), 221(3), 479-488
Open this publication in new window or tab >>Differential removal of human pathogenic viruses from sewage by conventional and ozone treatments
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2018 (English)In: International journal of hygiene and environmental health (Print), ISSN 1438-4639, E-ISSN 1618-131X, Vol. 221, no 3, p. 479-488Article in journal (Refereed) Published
Abstract [en]

Sewage contains a mixed ecosystem of diverse sets of microorganisms, including human pathogenic viruses. Little is known about how conventional as well as advanced treatments of sewage, such as ozonation, reduce the environmental spread of viruses. Analyses for viruses were therefore conducted for three weeks in influent, after conventional treatment, after additional ozonation, and after passing an open dam system at a full-scale treatment plant in Knivsta, Sweden. Viruses were concentrated by adsorption to a positively charged filter, from which they were eluted and pelleted by ultracentrifugation, with a recovery of about 10%. Ion Torrent sequencing was used to analyze influent, leading to the identification of at least 327 viral species, most of which belonged to 25 families with some having unclear classification. Real-time PCR was used to test for 21 human related viruses in inlet, conventionally treated, and ozone-treated sewage and outlet waters. The viruses identified in influent and further analyzed were adenovirus, norovirus, sapovirus, parechovirus, hepatitis E virus, astrovirus, pecovirus, picobirnavirus, parvovirus, and gokushovirus. Conventional treatment reduced viral concentrations by one to four log10, with the exception of adenovirus and parvovirus, for which the removal was less efficient. Ozone treatment led to a further reduction by one to two log10, but less for adenovirus. This study showed that the amount of all viruses was reduced by conventional sewage treatment. Further ozonation reduced the amounts of several viruses to undetectable levels, indicating that this is a promising technique for reducing the transmission of many pathogenic human viruses.

Place, publisher, year, edition, pages
Elsevier, 2018
Keywords
Waste water, Next generation sequencing, Effluent, Adenovirus, Parvovirus
National Category
Microbiology in the medical area
Identifiers
urn:nbn:se:umu:diva-151177 (URN)10.1016/j.ijheh.2018.01.012 (DOI)000438327900012 ()29402695 (PubMedID)2-s2.0-85041284211 (Scopus ID)
Available from: 2018-09-05 Created: 2018-09-05 Last updated: 2018-09-05Bibliographically approved
Saaristo, M., Brodin, T., Balshine, S., Bertram, M. G., Brooks, B. W., Ehlman, S. M., . . . Arnold, K. E. (2018). Direct and indirect effects of chemical contaminants on the behaviour, ecology and evolution of wildlife. Proceedings of the Royal Society of London. Biological Sciences, 285(1885), Article ID 20181297.
Open this publication in new window or tab >>Direct and indirect effects of chemical contaminants on the behaviour, ecology and evolution of wildlife
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2018 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 285, no 1885, article id 20181297Article, review/survey (Refereed) Published
Abstract [en]

Chemical contaminants (e.g. metals, pesticides, pharmaceuticals) are changing ecosystems via effects on wildlife. Indeed, recent work explicitly performed under environmentally realistic conditions reveals that chemical contaminants can have both direct and indirect effects at multiple levels of organization by influencing animal behaviour. Altered behaviour reflects multiple physiological changes and links individual-to population-level processes, thereby representing a sensitive tool for holistically assessing impacts of environmentally relevant contaminant concentrations. Here, we show that even if direct effects of contaminants on behavioural responses are reasonably well documented, there are significant knowledge gaps in understanding both the plasticity (i.e. individual variation) and evolution of contaminant-induced behavioural changes. We explore implications of multi-level processes by developing a conceptual framework that integrates direct and indirect effects on behaviour under environmentally realistic contexts. Our framework illustrates how sublethal behavioural effects of contaminants can be both negative and positive, varying dynamically within the same individuals and populations. This is because linkages within communities will act indirectly to alter and even magnify contaminant-induced effects. Given the increasing pressure on wildlife and ecosystems from chemical pollution, we argue there is a need to incorporate existing knowledge in ecology and evolution to improve ecological hazard and risk assessments.

Place, publisher, year, edition, pages
Royal Society, 2018
Keywords
behavioural ecology, endocrine-disrupting chemicals, predator-prey dynamics, plasticity, sublethal
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-151781 (URN)10.1098/rspb.2018.1297 (DOI)000443163500026 ()30135169 (PubMedID)
Funder
Swedish Research Council Formas, 2013-4431Swedish Research Council Formas, 2013-947Wenner-Gren Foundations
Available from: 2018-09-14 Created: 2018-09-14 Last updated: 2018-09-14Bibliographically approved
Pohl, J., Björlenius, B., Brodin, T., Carlsson, G., Fick, J., Larsson, D. G., . . . Örn, S. (2018). Effects of ozonated sewage effluent on reproduction and behavioral endpoints in zebrafish (Danio rerio). Aquatic Toxicology, 200, 93-101
Open this publication in new window or tab >>Effects of ozonated sewage effluent on reproduction and behavioral endpoints in zebrafish (Danio rerio)
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2018 (English)In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 200, p. 93-101Article in journal (Refereed) Published
Abstract [en]

Pharmaceutical residues and other micro-contaminants may enter aquatic environments through effluent from sewage treatment plants (STPs) and could cause adverse effects in wild fish. One strategy to alleviate this situation is to improve wastewater treatment by ozonation. To test the effectiveness of full-scale wastewater effluent ozonation at a Swedish municipal STP, the added removal efficiency was measured for 105 pharmaceuticals. In addition, gene expression, reproductive and behavioral endpoints were analyzed in zebrafish (Danio rerio) exposed on-site over 21 days to ozonated or non-ozonated effluents as well as to tap water. Ozone treatment (7 g O-3/m(3)) removed pharmaceuticals by an average efficiency of 77% in addition to the conventional treatment, leaving 11 screened pharmaceuticals above detection limits. Differences in biological responses of the exposure treatments were recorded in gene expression, reproduction and behavior. Hepatic vitellogenin gene expression was higher in male zebrafish exposed to the ozonated effluent compared to the non-ozonated effluent and tap water treatments. The reproductive success was higher in fish exposed to ozonated effluent compared to non-ozonated effluent and to tap water. The behavioral measurements showed that fish exposed to the ozonated STP effluent were less active in swimming the first minute after placed in a novel vessel. Ozonation is a capable method for removing pharmaceuticals in effluents. However, its implementation should be thoroughly evaluated for any potential biological impact. Future research is needed for uncovering the factors which produced the in vivo responses in fish.

Place, publisher, year, edition, pages
Elsevier, 2018
Keywords
Fecundity, Vitellogenin, Ozone, Pharmaceuticals, Wastewater
National Category
Other Biological Topics Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-150383 (URN)10.1016/j.aquatox.2018.04.014 (DOI)000438180700010 ()29729477 (PubMedID)2-s2.0-85046783086 (Scopus ID)
Available from: 2018-08-08 Created: 2018-08-08 Last updated: 2018-08-08Bibliographically approved
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