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Knigge T. Antidepressants - The new endocrine disruptors? The case of crustaceans. Mol Cell Endocrinol 2024; 583:112155. [PMID: 38185462 DOI: 10.1016/j.mce.2024.112155] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/15/2023] [Revised: 12/31/2023] [Accepted: 01/05/2024] [Indexed: 01/09/2024]
Abstract
Antidepressants are high-volume pharmaceuticals that accumulate to concentrations in the μg·L-1 range in surface waters. The release of peptide hormones via neurosecretory cells appears as a natural target for antidepressants. Here I review research that suggests that antidepressants indeed disrupt endocrine signalling in crustaceans, by acting on the synthesis and release of neurohormones, such as crustacean hyperglycaemic hormone, moult inhibiting hormone and pigment dispersing hormone in decapods, as well as methyl farnesoate in Daphnids. Hence, antidepressants can affect hormonal regulation of physiological functions: increase in energy metabolism and activity, lowered ecdysteroid levels, potentially disrupting moult and somatic growth, reducing colour change capacity and compromising camouflage, as well as induction of male sex determination. Several studies further suggest effects of antidepressants on crustacean reproduction, but the hormonal regulation of these effects remains elusive. All things considered, a body of evidence strongly suggests that antidepressants are endocrine disrupting compounds in crustaceans.
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Affiliation(s)
- Thomas Knigge
- Normandie Univ, Unilehavre, FR CNRS 3730 Sciences Appliquées à L'Environnement, UMR-I02, Environmental Stress and Biomonitoring of Aquatic Environments, University of Le Havre Normandy, France.
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Argaluza J, Domingo-Echaburu S, Orive G, Medrano J, Hernandez R, Lertxundi U. Environmental pollution with psychiatric drugs. World J Psychiatry 2021; 11:791-804. [PMID: 34733642 PMCID: PMC8546762 DOI: 10.5498/wjp.v11.i10.791] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/23/2021] [Revised: 06/25/2021] [Accepted: 08/31/2021] [Indexed: 02/06/2023] Open
Abstract
Among all contaminants of emerging interest, drugs are the ones that give rise to the greatest concern. Any of the multiple stages of the drug's life cycle (production, consumption and waste management) is a possible entry point to the different environmental matrices. Psychiatric drugs have received special attention because of two reasons. First, their use is increasing. Second, many of them act on phylogenetically highly conserved neuroendocrine systems, so they have the potential to affect many non-target organisms. Currently, wastewater is considered the most important source of drugs to the environment. Furthermore, the currently available wastewater treatment plants are not specifically prepared to remove drugs, so they reach practically all environmental matrices, even tap water. As drugs are designed to produce pharmacological effects at low concentrations, they are capable of producing ecotoxicological effects on microorganisms, flora and fauna, even on human health. It has also been observed that certain antidepressants and antipsychotics can bioaccumulate along the food chain. Drug pollution is a complicated and diffuse problem characterized by scientific uncertainties, a large number of stakeholders with different values and interests, and enormous complexity. Possible solutions consist on acting at source, using medicines more rationally, eco-prescribing or prescribing greener drugs, designing pharmaceuticals that are more readily biodegraded, educating both health professionals and citizens, and improving coordination and collaboration between environmental and healthcare sciences. Besides, end of pipe measures like improving or developing new purification systems (biological, physical, chemical, combination) that eliminate these residues efficiently and at a sustainable cost should be a priority. Here, we describe and discuss the main aspects of drug pollution, highlighting the specific issues of psychiatric drugs.
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Affiliation(s)
- Julene Argaluza
- Department of Epidemiology and Public Health, Bioaraba Health Research Institute, Vitoria-Gasteiz 01002, Spain
| | - Saioa Domingo-Echaburu
- Department of Pharmacy, Alto Deba Integrated Health Care Organization, Arrasate 20500, Spain
| | - Gorka Orive
- NanoBioCel Group, Laboratory of Pharmaceutics, School of Pharmacy, University of the Basque Country UPV/EHU, Paseo de la Universidad 7, Vitoria-Gasteiz 01006, Spain
- Biomedical Research Networking Centre in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Vitoria-Gasteiz 01006, Spain
- Bioaraba, NanoBioCel Research Group, Vitoria-Gasteiz 01006, Spain
- Singapore Eye Research Institute, Discovery Tower, Singapore 168751, Singapore
| | - Juan Medrano
- Department of Psychiatry, Biocruces Bizkaia Health Research Institute, Mental Health Network Research Group, Osakidetza, Portugalete 48920, Spain
| | - Rafael Hernandez
- Department of Internal Medicine, Araba Mental Health Network, Vitoria-Gasteiz 01006, Spain
| | - Unax Lertxundi
- Bioaraba Health Research Institute; Osakidetza Basque Health Service, Araba Mental Health Network, Araba Psychiatric Hospital, Pharmacy Service, Vitoria-Gasteiz 01006, Alava, Spain
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Polverino G, Martin JM, Bertram MG, Soman VR, Tan H, Brand JA, Mason RT, Wong BBM. Psychoactive pollution suppresses individual differences in fish behaviour. Proc Biol Sci 2021; 288:20202294. [PMID: 33563120 DOI: 10.1098/rspb.2020.2294] [Citation(s) in RCA: 23] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/15/2022] Open
Abstract
Environmental contamination by pharmaceuticals is global, substantially altering crucial behaviours in animals and impacting on their reproduction and survival. A key question is whether the consequences of these pollutants extend beyond mean behavioural changes, restraining differences in behaviour between individuals. In a controlled, two-year, multigenerational experiment with independent mesocosm populations, we exposed guppies (Poecilia reticulata) to environmentally realistic levels of the ubiquitous pollutant fluoxetine (Prozac). Fish (unexposed: n = 59, low fluoxetine: n = 57, high fluoxetine: n = 58) were repeatedly assayed on four separate occasions for activity and risk-taking behaviour. Fluoxetine homogenized individuals' activity, with individual variation in populations exposed to even low concentrations falling to less than half that in unexposed populations. To understand the proximate mechanism underlying these changes, we tested the relative contribution of variation within and between individuals to the overall decline in individual variation. We found strong evidence that fluoxetine erodes variation in activity between but not within individuals, revealing the hidden consequences of a ubiquitous contaminant on phenotypic variation in fish-likely to impair adaptive potential to environmental change.
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Affiliation(s)
- Giovanni Polverino
- Centre for Evolutionary Biology, School of Biological Sciences, The University of Western Australia (M092), 35 Stirling Highway, 6009 Perth, WA, Australia
| | - Jake M Martin
- School of Biological Sciences, Monash University, Australia
| | - Michael G Bertram
- School of Biological Sciences, Monash University, Australia.,Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, Sweden
| | - Vrishin R Soman
- Centre for Evolutionary Biology, School of Biological Sciences, The University of Western Australia (M092), 35 Stirling Highway, 6009 Perth, WA, Australia.,Department of Mechanical and Aerospace Engineering, New York University Tandon School of Engineering, USA
| | - Hung Tan
- School of Biological Sciences, Monash University, Australia
| | - Jack A Brand
- School of Biological Sciences, Monash University, Australia
| | - Rachel T Mason
- School of Biological Sciences, Monash University, Australia
| | - Bob B M Wong
- School of Biological Sciences, Monash University, Australia
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Ford AT, LeBlanc GA. Endocrine Disruption in Invertebrates: A Survey of Research Progress. ENVIRONMENTAL SCIENCE & TECHNOLOGY 2020; 54:13365-13369. [PMID: 33050691 DOI: 10.1021/acs.est.0c04226] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/06/2023]
Abstract
Manmade chemicals can interfere with endocrine processes and have permeated many ecosystems. Arguably, the most devastating example of endocrine disruption occurred in gastropod molluscs which led to the banning of tributyltin. The invertebrates consist of ∼95% of all known animals and possess endocrine systems that can significantly differ from that of vertebrates. An expert group in the late 1990s highlighted considerable paucity in our knowledge of these endocrine systems and the limited ability to ascertain risks of endocrine-disrupting chemicals (EDCs) to invertebrates. Twenty years later, we surveyed experts in this field on the current state of the science. Respondents agreed that endocrine disruption is still a significant issue and noted that there was key evidence that EDCs were impacting invertebrates groups. Respondents noted a variety of impediments to advancing the science, including inadequate funding, insufficient knowledge to develop appropriate assays, and generally low support for invertebrate studies. Several scientists highlighted that resources were being misdirected with studies that address impacts of vertebrate EDCs or using biomarkers specific to vertebrate endocrine disruption. Sadly, many of the recommendations proposed by respondents matched those made over two decades ago. Accordingly, the field has not advanced as much as one might have expected.
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Affiliation(s)
- Alex T Ford
- Institute of Marine Sciences, School of Biological Sciences, University of Portsmouth, Ferry Road, Portsmouth, Hampshire PO4 9LY, United Kingdom
| | - Gerald A LeBlanc
- Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina 27695, United States
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Ford AT. Comment on "Principles of Sound Ecotoxicology". ENVIRONMENTAL SCIENCE & TECHNOLOGY 2017; 51:11493-11495. [PMID: 28925258 DOI: 10.1021/acs.est.7b03385] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/07/2023]
Affiliation(s)
- Alex T Ford
- Institute of Marine Sciences, School of Biological Sciences, University of Portsmouth , Ferry Road, Portsmouth, PO4 9LY, United Kingdom
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Ford AT, Fong PP. The effects of antidepressants appear to be rapid and at environmentally relevant concentrations. ENVIRONMENTAL TOXICOLOGY AND CHEMISTRY 2016; 35:794-8. [PMID: 26031210 DOI: 10.1002/etc.3087] [Citation(s) in RCA: 81] [Impact Index Per Article: 9.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/27/2015] [Revised: 04/15/2015] [Accepted: 05/26/2015] [Indexed: 05/11/2023]
Abstract
The effects of antidepressants on wildlife are currently raising some concern because of an increased number of publications indicating biological effects at environmentally relevant concentrations (<100 ng/L). These results have been met with some scepticism because of the higher concentrations required to detect effects in some species and the perceived slowness to therapeutic effects recorded in humans and other vertebrates. Because their mode of action is thought to be by modulation of the neurotransmitters serotonin, dopamine, and norepinephrine, aquatic invertebrates that possess transporters and receptors sensitive to activation by these pharmaceuticals are potentially affected by them. The authors highlight studies on the effects of antidepressants, particularly on crustacean and molluskan groups, showing that they are susceptible to a wide variety of neuroendocrine disruptions at environmentally relevant concentrations. Interestingly, some effects observed in these species can be observed within minutes to hours of exposure. For example, exposure of amphipod crustaceans to several selective serotonin reuptake inhibitors can invoke changes in swimming behavior within hours. In mollusks, exposure to selective serotonin reuptake inhibitors can induce spawning in male and female mussels and foot detachment in snails within minutes of exposure. In the light of new studies indicating effects on the human brain from selective serotonin reuptake inhibitors using magnetic resonance imaging scans, the authors discuss possible reasons for the discrepancy in former results in relation to the read-across hypothesis, variation in biomarkers used, modes of uptake, phylogenetic distance, and the affinity to different targets and differential sensitivity to receptors.
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Affiliation(s)
- Alex T Ford
- Institute of Marine Sciences, School of Biological Sciences, University of Portsmouth, Ferry Road, Portsmouth, United Kingdom
| | - Peter P Fong
- Department of Biology, Gettysburg College, Gettysburg, Pennsylvania, USA
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Arnold KE, Brown AR, Ankley GT, Sumpter JP. Medicating the environment: assessing risks of pharmaceuticals to wildlife and ecosystems. Philos Trans R Soc Lond B Biol Sci 2015; 369:rstb.2013.0569. [PMID: 25405959 DOI: 10.1098/rstb.2013.0569] [Citation(s) in RCA: 256] [Impact Index Per Article: 25.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/12/2022] Open
Abstract
Global pharmaceutical consumption is rising with the growing and ageing human population and more intensive food production. Recent studies have revealed pharmaceutical residues in a wide range of ecosystems and organisms. Environmental concentrations are often low, but pharmaceuticals typically are designed to have biological effects at low doses, acting on physiological systems that can be evolutionarily conserved across taxa. This Theme Issue introduces the latest research investigating the risks of environmentally relevant concentrations of pharmaceuticals to vertebrate wildlife. We take a holistic, global view of environmental exposure to pharmaceuticals encompassing terrestrial, freshwater and marine ecosystems in high- and low-income countries. Based on both field and laboratory data, the evidence for and relevance of changes to physiology and behaviour, in addition to mortality and reproductive effects, are examined in terms of the population- and community-level consequences of pharmaceutical exposure on wildlife. Studies on uptake, trophic transfer and indirect effects of pharmaceuticals acting via food webs are presented. Given the logistical and ethical complexities of research in this area, several papers focus on techniques for prioritizing which compounds are most likely to harm wildlife and how modelling approaches can make predictions about the bioavailability, metabolism and toxicity of pharmaceuticals in non-target species. This Theme Issue aims to help clarify the uncertainties, highlight opportunities and inform ongoing scientific and policy debates on the impacts of pharmaceuticals in the environment.
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Affiliation(s)
| | - A Ross Brown
- AstraZeneca Safety, Health and Environment, Brixham Environmental Laboratory, Brixham, UK University of Exeter, Biosciences, College of Life and Environmental Sciences, Exeter, UK
| | | | - John P Sumpter
- Institute for the Environment, Brunel University, Uxbridge, UK
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