Abstract
Cyanobacteria are important for ecosystem functioning, but eutrophication may affect the surrounding biome by losing ecosystem services and/or through affecting the cyanotoxins production that threatens ecological and human health. Pollution is an environmental issue that affects aquatic ecosystems worldwide, and the knowledge of the role of synthetic chemicals such as pharmaceuticals is still scarce. Therefore, studies coupling these two relevant issues are essential to better understand the ecological risks and the potential threats to public health. Thus, an overview of ecotoxicological tests performed in the literature exposing cyanobacteria to pharmaceuticals and the possible consequences regarding ecological and sanitary aspects was conducted. Moreover, a risk assessment was performed to enable a better understanding of pharmaceuticals affecting cyanobacteria ecology. Most of the studies found in the literature tested isolated pharmaceuticals in laboratory conditions, while others assessed mixture effects on in situ conditions. The endpoints most assessed were growth, photosynthesis, and antioxidant enzyme activity. The studies also point out that cyanobacteria may present resistance or sensitivity depending on the concentrations and the therapeutic class, which may cause a change in the ecosystem dynamics and/or sanitary implications due to cyanotoxin production. The risk assessment highlighted that antibiotics are among the most relevant substances due to the chemical diversity and higher levels found in the environment than other therapeutic classes. This review highlighted gaps regarding cyanotoxin release into aquatic environments due to the occurrence of pharmaceuticals and the need for more realistic experiments to better understand the potential consequences for human and environmental health.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
References
ANA (2017) Agência Nacional das Águas (Brasil). Atlas sewers: watershed 879 depollution (In Portuguese). http://atlasesgotos.ana.gov.br/
Ando T, Nagase H, Eguchi K, Hirooka T, Nakamura T, Miyamoto K, Hirata (2007) A novel method using cyanobacteria for ecotoxicity test of veterinary antimicrobial agentes. Envron Toxicol Chem 26:601–609. https://doi.org/10.1897/06-195r.1
Aquino SFD, Brandt EMF, Chernicharo CADL (2013) Removal of pharmaceuticals and endocrine disrupters in sewage treatment plants: literature review. In Portuguese. Eng Sanit Ambient 18:187–204. https://doi.org/10.1590/S1413-41522013000300002
Aris AZ, Shamsuddin AS, Praveena SM (2014) Occurrence of 17α-ethynylestradiol (EE2) in the environment and effect on exposed biota: a review. Environ Int 69:104–119. https://doi.org/10.1016/j.envint.2014.04.011
Arnold KE, Brown AR, Ankley GT, Sumpter JP (2014) Medicating the environment: assessing risks of pharmaceuticals to wildlife and ecosystems. Philos Trans R Soc B 369:1–11. https://doi.org/10.1098/rstb.2013.0569
Azevedo SMOF, Carmichael WW, Jochimsen EM, Rinehart KL, Lau S, Shaw GR, Eaglesham GK (2002) Human intoxication by microcystins during renal dialysis treatment in Caruaru—Brazil. Toxicology 181:441–446. https://doi.org/10.1016/s0300-483x(02)00491-2
Bácsi I, Bére V B, Kókia Z, Gonda S, Novák Z, Nagy SA, Vasas G (2016) Efeitos of non-asteroidal anti-inflammatory drugs on cyanobacteria and algae in laboratory strains and in natural algal assemblages. Environ Pollut 212:508–518. https://doi.org/10.1016/j.envpol.2016.02.031
Baker DR, Kasprzyk-Hordern B (2013) Spatial and temporal occurrence of pharmaceuticals and illicit drugs in the aqueous environment and during wastewater treatment: new developments. Sci Total Environ 454:442–456. https://doi.org/10.1016/j.scitotenv.2013.03.043
Barrios-Estrada C, Rostro-Alanis MDJ, Muñoz-Gutiérrez BD, Iqbal HMN, Kannan S, Parra-Saldívar R (2018) Emergent contaminants: endocrine disruptors and their laccase-assisted degradation – a review. Sci Total Environ 612:1516–1531. https://doi.org/10.1016/j.scitotenv.2017.09.013
Baumann M, Weis K, Maletzki D, Schüssler W, Schudoma D, Kopf W, Kühnen U (2015) Aquatic toxicity of the macrolide antibiotic clarithromycin and its metabolites. Chemosphere 120:192–198. https://doi.org/10.1016/j.chemosphere.2014.05.089
Benotti MJ, Trenholm RA, Vanderford BJ, Holady JC, Stanford BD, Snyder SA (2009) Pharmaceuticals and endocrine disrupting compounds in U.S. drinking water. Environ Sci Technol 43:597–603. https://doi.org/10.1016/10.1021/es801845a
Beretta M, Britto V, Tavares TM, Silva SMTD, Pletsch AL (2014) Occurrence of pharmaceutical and personal care products (PPCPs) in marine sediments in the Todos os Santos Bay and the north coast of Salvador. Bahia, Brazil J Soils Sediments 14:1278–1286. https://doi.org/10.1007/s11368-014-0884-6
Biel-Maeso M, Corada-Fernández C, Lara-Martín PA (2018) Monitoring the occurrence of pharmaceuticals in soil irrigated with reclaimed wastewater. Environ Pollut 235:312–212. https://doi.org/10.1016/j.envpol.2017.12.085
Bound JP, Voulvoulis N (2005) Household Disposal of Pharmaceuticals as a Pathway for Aquatic Contamination in the United Kingdom. Environ Health Perspect 113:1705–1711. https://doi.org/10.1289/ehp.8315
Brezovšek P, Eleršek T, Filipiĉ M (2014) Toxicities of four anti-neoplastic drugs and their binary mixtures tested on the green alga Pseudokirchneriella subcapitata and the cyanobacterium Synechococcus leopoliensis. Water Res 52:168–177. https://doi.org/10.1016/j.watres.2014.01.007
Burch KD, Han B, Pichtel J, Zubkov T (2019) Removal efficiency of commonly prescribed antibiotics via tertiary wastewater treatment. Environ Sci Pollut Res 26:6301–6310. https://doi.org/10.1007/s11356-019-04170-w
Caban M, Stepnowski P (2021) How to decrease pharmaceuticals in the environment? A review. Environ Chem Lett. https://doi.org/10.1007/s10311-021-01194-y
Carlsson C, Johansson A-K, Alvan G, Bergman K, Kühler T (2006) Are pharmaceuticals potent environmental pollutants? Part I: Environmental risk assessments of selected active pharmaceutical ingredients. Sci Total Environ 364:67–87. https://doi.org/10.1016/j.scitotenv.2005.06.035
Christen V, Hickmann S, Rechenberg B, Fent K (2010) Highly active human pharmaceuticals in aquatic systems: a concept for their identification based on their mode of action. Aquat Toxicol 96:167–181. https://doi.org/10.1016/j.aquatox.2009.11.021
Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272. https://doi.org/10.1016/j.taap.2004.02.016
Corcoll N, Acunã V, Barceló D, Casellas M, Guasch H, Huerta B, Petrovic M, Ponsatí L, Rodríguez-Mozaz S, Sabater S (2014) Pollution-induced community tolerance to non-steroidal anti-inflammatory drugs (NSAIDs) in fluvial biofilm communities affected by WWTP effluents. Chemosphere. 112:185–193. https://doi.org/10.1016/j.chemosphere.2014.03.128
Crane M, Watts C, Boucard T (2006) Chronic aquatic environmental risks from exposure to human pharmaceuticals. Sci Total Environ 367:23–41. https://doi.org/10.1016/j.scitotenv.2006.04.010
Cunningham VL, Buzby M, Hutchinson T, Mastrocco F, Parke N, Roden N (2006) Effects of human pharmaceuticals on aquatic life: next steps. Environ Sci Technol 11:3456–3462. https://doi.org/10.1021/es063017b
De Lange HJ, Noordoven W, Murk AJ, Lürling M, Peeters ETHM (2006) Behavioural responses of Gammarus pulex (Crustacea, Amphipoda) to low concentrations of pharmaceuticals. Aquat Toxicol 78:209–216. https://doi.org/10.1016/j.aquatox.2006.03.002
Desbiolles F, Malleret L, Tiliacos C, Wong-Wah-Chung P, Laffont-Schwob I (2018) Occurrence and ecotoxicological assessment of pharmaceuticals: is there a risk for the Mediterranean aquatic environment? Sci Total Environ 639:1334–1348. https://doi.org/10.1016/j.scitotenv.2018.04.351
Dias E, Oliveira M, Jones-Dias D, Vasconcelos V, Ferreira E, Manageiro V, Cania M (2015) Assessing the antibiotic susceptibility of freshwater Cyanobacteria spp. Front Microbiol 6:799. https://doi.org/10.3389/fmicb.2015.00799
Drobac D, Tokodi N, Lujić J, Marinović Z, Subakov-Simić G, Dulić T, Važić T, Nybom S, Meriluoto J, Codd GA, Svirčev Z (2016) Cyanobacteria and cyanotoxins in fishponds and their effects on fish tissue. Harmful Algae 55:66–76. https://doi.org/10.1016/j.hal.2016.02.007
Drury B, Scott J, Rosi-Marshall E, Kelly JJ (2013) Triclosan exposure increases triclosan resistance and influences taxonomic composition of benthic bacterial communities. Environ Sci Technol 47:8923–8930. https://doi.org/10.1021/es401919k
Du Y, Wang J, Zhu F, Mai D, Xiang Z, Chen J, Guo R (2018) Comprehensive assessment of three typical antibiotics on cyanobacteria (Microcystis aeruginosa): the impact and recovery capability. Ecotoxicol Environ Saf 160:84–93. https://doi.org/10.1016/j.ecoenv.2018.05.035
Dussault EB, Balakrishnan V, Ed S, Solomon KR, Silbley PK (2008) Toxicity of human pharmaceuticals and personal care products to benthic invertebrates. Environ Toxicol Chem 27:425–432. https://doi.org/10.1897/07-354R.1
Ebert I, Bachmann J, Kühnen U, Küster A, Kussatz C, Maletzki D, Schlüter C (2011) Toxicity of the fluoroquinolone antibiotics enrofloxacin and ciprofloxacin to photoautotrophic aquatic organisms. Environ Toxicol Chem 30:2786–2792. https://doi.org/10.1002/etc.678
Eriksson KM, Johansson CH, Fihlan V, Grehn A, Sanli K, Andersson MX, Blanck H, Arrhenius A, Sircar T, Backhaus T (2015) Long-term effects of the antibacterial agent triclosan on marine periphyton communities. Environ Toxicol Chem 34:2067–2077. https://doi.org/10.1002/etc.3030
Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76:122–159. https://doi.org/10.1016/j.aquatox.2005.09.009
Franzellitti S, Buratti S, Valbonesi P, Fabbri E (2013) The mode of action (MOA) approach reveals interactive effects of environmental pharmaceuticals on Mytilus galloprovincialis. Aquat Toxicol 140-141:249–256. https://doi.org/10.1016/j.aquatox.2013.06.005
Froehner K, Backhaus T, Grimme LH (2000) Bioassays with Vibrio fischeri for the assessment of delayed toxicity. Chemosphere. 40:821–828. https://doi.org/10.1016/s0045-6535(99)00274-x
Funari E, Testai E (2008) Human health risk assessment related to cyanotoxins exposure. Crit Rev Toxicol 38:97–125. https://doi.org/10.1080/10408440701749454
Giannuzzi L, Sedan D, Echenique R, Andrinolo D (2011) An acute case of intoxication with cyanobacteria and cyanotoxins in recreational water in Salto Grande Dam, Argentina. Mar Drugs 9:2164–2217. https://doi.org/10.3390/md9112164
Gogoi A, Mazumder P, Tyagi VK, Chaminda GGT, An AK, Kumar M (2018) Occurrence and fate of emerging contaminants in water environment: a review. Groundw Sustain Dev 6:169–180. https://doi.org/10.1016/j.gsd.2017.12.009
González-Pleiter M, Gonzalo S, Rodea-Palomares I, Leganés F, Rolsa R, Boltes K, Marco E, Fernández-Piñas F (2013) Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: implications for environmental risk assessment. Water Res 47:2050–2064. https://doi.org/10.1016/j.watres.2013.01.020
Guo J, Selby K, Boxall ABA (2016) Effects of antibiotics on the growth and physiology of chlorophytes, cyanobacteria, and a diatom. Arch Environ Contam Toxicol 71:589–602. https://doi.org/10.1007/s00244-016-0305-5
Halling-Sørensen B (2000) Algal toxicity of antibacterial agents used in intensive farming. Chemosphere. 40:731–739. https://doi.org/10.1016/S0045-6535(99)00445-2
Hamscher G, Pawelzick HT, Höper H, Nau H (2004) Antibiotics in soil: routes of entry, environmental concentrations, fate and possible effects. In: Kümmerer K (ed) Pharmaceuticals in the environment. Springer, Berlin, Heidelberg, pp 139–147
Harke MJ, Steffen MM, Golber CJ, Otten TG, Wilhelm SW, Wood SA, Paerl HW (2016) A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54:4–20. https://doi.org/10.1016/j.hal.2015.12.007
Harrass MC, Kindig AC, Taub FB (1985) Responses of blue-green and green algae to streptomycin in unialgal and paired culture. Aquat Toxicol 6:1–11. https://doi.org/10.1016/0166-445X(85)90015-3
Hense BA, Jaser W, Welzl G, Pfister G, Wöhler-Moorhoff GF, Schramm K-W (2008) Impact of 17α-ethinylestradiol on the plankton in freshwater microcosms—II: Responses of phytoplankton and the interrelation within the ecosystem. Ecotox. Environ Saf 69:453–465. https://doi.org/10.1016/j.ecoenv.2007.01.014
Hoeger B, Köllner B, Dietrich DR, Hitzfeld B (2005) Water-borne diclofenac affects kidney and gill integrity and selected immune parameters in brown trout (Salmo trutta f. fario). Aquat Toxicol 75:53–64. https://doi.org/10.1016/j.aquatox.2005.07.006
Huang X, Tu Y, Song C, Li T, Lin J, Wu Y, Liu J, Wu C (2016) Interactions between the antimicrobial agent triclosan and the bloom-forming cyanobacteria Microcystis aeruginosa. Aquat Toxicol 72:103–110. https://doi.org/10.1016/j.aquatox.2016.01.002
Huisman J, Codd GA, Paerl HW, Ibelings BW, Verspagen JMH, Visser PM (2018) Cyanobacterial blooms. Nat Rev Microbiol 16:471–483. https://doi.org/10.1038/s41579-018-0040-1
Humbert J-F, Barbe V, Latifi A, Gugger M, Calteau A, Coursin T, Lajus A, Castelli V, Oztas S, Samson G, Longin C, Medique C, de Marsac NT (2013) A tribute to disorder in the genome of the bloom-forming freshwater cyanobacterium Microcystis aeruginosa. PLoS One 8:e70747. https://doi.org/10.1371/journal.pone.0070747
Jones OAH, Voulvoulis N, Lester JN (2004) Potential ecological and human health risks associated with the presence of pharmaceutically active compounds in the aquatic environment. Crit Ver Toxicol 34:335–350. https://doi.org/10.1080/10408440490464697
Kasprzyk-Hordern B, Dinsdale RM, Guwy AJ (2008) The occurrence of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs in surface water in South Wales, UK. Water Res 48:3498–3518. https://doi.org/10.1016/j.watres.2008.04.026
Kim Y, Choi K, Jung J, Park S, Kim P-G, Park J (2007) Aquatic toxicity of acetaminophen, carbamazepine, cimetidine, diltiazem and six major sulfonamides, and their potential ecological risks in Korea. Environ Int 33:370–374. https://doi.org/10.1016/j.envint.2006.11.017
Kolar B, Arnuš L, Jeretin B, Gutmaher A, Drobne D, Durjava MK (2014) The toxic effect of oxytetracycline and trimethoprim in the aquatic environment. Chemosphere. 115:75–80. https://doi.org/10.1016/j.chemosphere.2014.02.049
K'oreje KO, Vergeynst L, Ombaka D, De Wispelaere P, Okoth M, Van Langenhove H, Demeestere K (2016) Occurrence patterns of pharmaceutical residues in wastewater, surface water and groundwater of Nairobi and Kisumu city, Kenya. Chemosphere 149:238–244. https://doi.org/10.1016/j.chemosphere.2016.01.095
Kosma CI, Lambropoulou DA, Albanis TA (2014) Investigation of PPCPs in wastewater treatment plants in Greece: occurrence, removal and environmental risk assessment. Sci Total Environ 466:421–438. https://doi.org/10.1016/j.scitotenv.2013.07.044
Kumar HD (1965) Effects of certain toxic chemicals and mutagens on the growth of the blue-green alga Anacystis nidulans. Can J Bot 43:1523–1532. https://doi.org/10.1139/b65-161
Kümmerer K (2009) Antibiotics in the aquatic environment–a review–part I. Chemosphere 75:417–434. https://doi.org/10.1016/j.chemosphere.2008.11.086
Kvíderová J, Henley WJ (2005) The effect of ampicillin plus streptomycin on growth and photosynthesis of two halotolerant chlorophyte algae. J Appl Psychol 17:301–307. https://doi.org/10.1007/s10811-005-7293-6
Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113–390 https://10.1080/20026491051695
Lawrence JR, Swerhone GDW, Wassenaar LI, Neu TR (2005) Effects of selected pharmaceuticals on riverine biofilm communities. Can J Microbiol 51:655–669. https://doi.org/10.1139/w05-047
Lawrence JR, Swerhone GDW, Topp E, Korber DR, Neu TR, Wassenaar LI (2007) Structural and functional responses of river biofilm communities to the non-steroidal anti-inflammatory diclofenac. Environ Toxicol Chem 26:573–582. https://doi.org/10.1897/06-340r.1
Lawrence JR, Zhu B, Swerhone GDW, Roy J, Tumber V, Waiser MJ, Topp E, Korber DR (2012) Molecular and microscopic assessment of the effects of caffeine, acetaminophen, diclofenac, and their mixtures on river biofilm communities. Environ Toxicol Chem 1:508–517. https://doi.org/10.1002/etc.1723
Le Page G, Gunnarsson L, Trznadel M, Wedgwood KCA, Baudrot V, Snape J, Tyler CR (2019) Variability in cyanobacteria sensitivity to antibiotics and implications for environmental risk assessment. Sci Total Environ 695:133804. https://doi.org/10.1016/j.scitotenv.2019.133804
Li Y, Han XD (2012) Microcystin–LR causes cytotoxicity effects in rat testicular Sertoli cells. Environ Toxicol Pharmacol 33:318–326. https://doi.org/10.1016/j.etap.2011.12.015
Liguoro MD, Fioretto B, Poltronieri C, Gallina G (2009) The toxicity of sulfamethazine to Daphnia magna and its additivity to other veterinary sulfonamides and trimethoprim. Chemosphere 75:1519–1524. https://doi.org/10.1016/j.chemosphere.2009.02.002
Liguoro MD, Di Leva V, Gallina G, Faccio E, Pinto G, Pollio A (2010) Evaluation of the aquatic toxicity of two veterinary sulfonamides using five test organisms. Chemosphere 81:788–793. https://doi.org/10.1016/j.chemosphere.2010.07.003
Liu Y, Gao B, Yue Q, Guan Y, Wang Y, Huang L (2012) Influences of two antibiotic contaminants on the production, release and toxicity of microcystins. Ecotoxicol Environ Saf 77:79–87. https://doi.org/10.1016/j.ecoenv.2011.10.027
Liu Y, Zhang J, Gao B, Feng S (2014) Combined effects of two antibiotic contaminants on Microcystis Aeruginosa. J Hazard Mater 160:84–93. https://doi.org/10.1016/j.ecoenv.2018.05.035
Liu Y, Chen X, Zhang J, Gao B (2015) Hormesis effects of amoxicillin on growth and cellular biosynthesis of Microcystis aeruginosa at different nitrogen levels. Microb Ecol 69:608–617. https://doi.org/10.1007/s00248-014-0528-9
Liu Y, Chen S, Zhang J, Gao B (2016) Growth, microcystin-production and proteomic responses of Microcystis aeruginosa under long-term exposure to amoxicillin. Water Res 93:141–152 https://doi.org/10.1016/j.watres.2016.01.060
Lützhøft H-CH, Halling-Sørensen B, Jørgensen SE (1999) Algal toxicity of antibacterial agents applied in danish fish farming. Arch Environ Contam Toxicol 36:1–6. https://doi.org/10.1007/s002449900435
Magalhães VD, Marinho MM, Domingos P, Oliveira AC, Costa SM, Azevedo LOD, Azevedo SMFO (2003) Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brasil, RJ). Toxicon 42:289–295. https://doi.org/10.1016/S0041-0101(03)00144-2
Magalhães SMS, Brêtas CM, Brêtas JM, Pianetti GA, Franco MW, Barbosa FAR (2014) Toxic concentrations of metronidazole to Microcystis protocystis. Braz J Biol 74:S120–S124. https://doi.org/10.1590/1519-6984.03513
Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902. https://doi.org/10.1016/j.envpol.2009.05.051
Matongo S, Birungi G, Moodley B, Ndungu P (2015) Pharmaceutical residues in water and sediment of Msunduzi River, KwaZulu-Natal, South Africa. Chemosphere 134:133–140. https://doi.org/10.1016/j.chemosphere.2015.03.093
Matthijs HCP, Jančula D, Visser PM, Maršálek B (2016) Existing and emerging cyanocidal compounds: new perspectives for cyanobacterial bloom mitigation. Aquat Ecol 50:443–460. https://doi.org/10.1007/s10452-016-9577-0
Merel S, Walker D, Chicana R, Snyder S, Baurès E, Thomas O (2013) State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int 59:303–327. https://doi.org/10.1016/j.envint.2013.06.013
Moore BS (1999) Biosynthesis of marine natural products: microorganisms and macroalgae. Nat Prod Rep 16:653–674. https://doi.org/10.1039/A805873C
Nietch CT, Quinlan EL, Lazorchak J, Impellitteri C, Raikow D, Walters DM (2013) Effects of a chronic lower range of triclosan exposure on a stream mesocosm community. Environ Toxicol Chem 32:2874–2887. https://doi.org/10.1002/etc.2385
Obimakinde S, Fatoki O, Opeolu B, Olatunji O (2017) Veterinary pharmaceuticals in aqueous systems and associated effects: an update. Environ Sci Pollut Res 24:3274–3297. https://doi.org/10.1007/s11356-016-7757-z
Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010. https://doi.org/10.1007/s00248-012-0159-y
Pan X, Deng C, Zhang D, Wang J, Mu G, Chen Y (2008) Toxic effects of amoxicillin on the photosystem II of Synechocystis sp. characterized by a variety of in vivo chlorophyll fluorescence tests. Aquat Toxicol 89:207–213. https://doi.org/10.1016/j.aquatox.2008.06.018
Papageorgiou M, Kosma C, Lambropoulou D (2016) Seasonal occurrence, removal, mass loading and environmental risk assessment of 55 pharmaceuticals and personal care products in a municipal wastewater treatment plant in Central Greece. SciTotal Environ 543:547–569. https://doi.org/10.1016/j.scitotenv.2015.11.047
Perron M-C, Junaeu P (2011) Effect of endocrine disrupters on photosystem II energy fluxes of green algae and cyanobacteria. Environ Res 111:520–529. https://doi.org/10.1016/j.envres.2011.02.013
Pinckney JL, Hagenbuch IM, Long RA, Lovell CR (2013) Sublethal effects of the antibiotic tylosin on estuarine benthic microalgal communities. Mar Pollut Bull 68:8–12. https://doi.org/10.1016/j.marpolbul.2013.01.006
Pomati F, Neilan BA, Suzuki T, Manarolla G, Rossetti C (2003) Enhancement of intracellular saxitoxin accumulation by lidocaine hydrochloride in the cyanobacterium Cylindrospermopsis raciborskii t3 (nostocales). J Phycol 39:535–542. https://doi.org/10.1046/j.1529-8817.2003.02122.x
Pomati F, Netting AG, Calamari D, Neilan BA (2004) Effects of erythromycin, tetracycline and ibuprofen on the growth of Synechocystis sp. and Lemna minor. Aquat Toxicol 67:387–396. https://doi.org/10.1016/j.aquatox.2004.02.001
Pouria S, Andrade AD, Barbosa J, Cavalcanti RL, Barreto VT, Ward CJ, Preiser W, Poon GK, Neild GH, Codd GA (1998) Fatal microcystin intoxication in haemodialysis unit in Caruaru. Brazil Lancet 352:21–26. https://doi.org/10.1016/s0140-6736(97)12285-1
Proia L, Osorio V, Soley S, Köck-Schulmeyer M, Pérez S, Barceló D, Romaní AM, Sabater S (2013) Effects of pesticides and pharmaceuticals on biofilms in a highly impacted river. Environ Pollut 178:220–228. https://doi.org/10.1016/j.envpol.2013.02.022
Puckowski A, Mioduszewska K, Łukaszewicz P, Borecka M, Caban M, Maszkowska J, Stepnowski P (2016) Bioaccumulation and analytics of pharmaceutical residues in the environment: a review. J Pharm Biomed Anal 127:232–255. https://doi.org/10.1016/j.jpba.2016.02.049
Qian H, Li J, Pan X, Sun Z, Ye C, Jin G, Fu Z (2010) Effects of streptomycin on growth of algae Chlorella vulgaris and Microcystis aeruginosa. Environ Toxicol 27:229–237. https://doi.org/10.1002/tox.20636
Quadra GR, Souza HOD, Costa RDS, Fernadez MADS (2017) Do medicines reach and affect the aquatic ecosystems in Brazil? A critical review of current studies in a developing country. Environ. Scie Pollu Res 24:1200–1218. https://doi.org/10.1007/s11356-016-7789-4
Quadra GR, Silva PSA, Paranaíba JR, Josué IIP, Souza H, Costa R, Fernandez M, Vilas-Boas J, Roland F (2019) Investigation of medicines consumption and disposal in Brazil: a study case in a developing country. Sci Total Environ 671:505–509. https://doi.org/10.1016/j.scitotenv.2019.03.334
Rastogi PR, Sinha RP, Incharoensakdi A (2014) The cyanotoxin-microcystins: current overview. Rev Environ Sci Biotechnol 13:215–249. https://doi.org/10.1007/s11157-014-9334-6
Reis EO, Foureaux AFS, Rodrigues JS, Moreira VR, Lebron YAR, Santos LVS, Amaral MCS, Lange LC (2019) Occurrence, removal and seasonal variation of pharmaceuticals in Brasilian drinking water treatment plants. Environ Pollut 250:773–781. https://doi.org/10.1016/j.envpol.2019.04.102
Richards SM, Wilson CJ, Johnson DJ, Castle DM, Lam M, Mabury SA, Sibley PK, Solomon KR (2004) Effects of pharmaceutical mixtures in aquatic microcosms. Environ Toxicol Chem 23:1035–1042. https://doi.org/10.1897/02-616
Richardson SD, Kimura SY (2017) Emerging environmental contaminants: challenges facing our next generation and potential engineering solutions. Environ Technol Innov 8:40–56. https://doi.org/10.1016/j.eti.2017.04.002
Robinson AA, Belden JB, Lydy MJ (2005) Toxicity of fluoroquinolone antibiotics to aquatic organism. Environ Toxicol Chem 24:423–430. https://doi.org/10.1897/04-210r.1
Saker ML, Thomas AD, Norton JH (1999) Cattle mortality attributed to the toxic cyanobacterium Cylindrospermopsis raciborskii in an outback region of north Queensland. Environ Toxicol Int J 14:179–182. https://doi.org/10.1002/(SICI)1522-7278(199902)14:1<179::AID-TOX23>3.0.CO;2-G
Shang AH, Ye J, Chen DH, Lu XX, Lu HD, Liu CN, Wang LM (2015) Physiological effects of tetracycline antibiotic pollutants on non-target aquatic Microcystis aeruginosa. J Environ Sci Health B 50:809–818. https://doi.org/10.1080/03601234.2015.1058100
Sivonen K, Jones G (1999) Cyanobacterial toxins. Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. The World Health Organization/E and FN Spon
Stoichev T, Baptista MS, Basto MCP, Vasconcelos VM, Vasconcelos MTSD (2011) Effects of minocycline and its degradation products on the growth of Microcystis Aeruginosa. Ecotoxicol Environ Saf 74:219–224. https://doi.org/10.1016/j.ecoenv.2010.10.015
Suzuki T, Nakasato K, Shapiro S, Neilan BA (2004a) Effects of synthetic local anaesthetics on the growth of the cyanobacterium Synechococcus leopoliensis. J Appl Phycol 16:145–152. https://doi.org/10.1023/B:JAPH.0000044776.04977.00
Suzuki T, Shapiro S, Nagano A (2004b) Effects of bioactive substances on the growth of lithotrophic ammonia-oxidizing bacteria. J Toyo Uni Nat Sci 48:11–18. https://doi.org/10.34428/00002486
Teixeira MGLC, Costa MDCN, Carvalho VLPD, Pereira MDS, Hage E (1993) Epidemic of gastroenteritis in the Itaparica dam area, Bahia. (In Portuguese). Bol of Sanit Panam 114:244–253
Tijani JO, Fatoba OO, Babajide OO, Petrik LF (2016) Pharmaceuticals, endocrine disruptors, personal care products, nanomaterials and perfluorinated pollutants: a review. Environ Chem Lett 14:27–49. https://doi.org/10.1007/s10311-015-0537-z
Torres NH, Aguiar MM, Ferreira LFR, Américo JHP, Machado AM, Cavalcanti EB, Tornisielo VL (2015) Detection of hormones in surface and drinking water in Brazil by LC-ESI-MS/MS and ecotoxicological assessment with Daphnia magna. Environ Monit Assess 18:379. https://doi.org/10.1007/s10661-015-4626-z
UBA DATABASE (2018) https://www.umweltbundesamt.de/en/database-pharmaceuticals-in-the-environment-1.
Välitalo P, Kruglova A, Mikola A, Vahala R (2017) Toxicological impacts of antibiotics on aquatic microorganisms: a mini-review. Int J Hyg Environ Health 220:558–569. https://doi.org/10.1016/j.ijheh.2017.02.003
Van Buynder PG, Oughtred T, Kirkby B, Phillips S, Eaglesham G, Thomas K, Burch M (2001) Nodularin uptake by seafood during a cyanobacterial bloom. Environ Toxicol 16:468–471. https://doi.org/10.1002/tox.10004.abs
van der Grinten E, Pikkemaat MG, E-Jvd B, Stroomberg GJ, Kraak MHS (2010) Comparing the sensitivity of algal, cyanobacterial and bacterial bioassay to different groups of antibiotics. Chemosphere 80:1–6. https://doi.org/10.1016/j.chemosphere.2010.04.011
Vareli K, Jaeger W, Touka A, Frillingos S, Briasoulis E, Sainis I (2013) Hepatotoxic seafood poisoning (HSP) due to microcystins: a threat from the ocean? Mar Drugs 11:751–2768. https://doi.org/10.3390/md11082751
Wan J, Guo P, Peng X, Wen K (2015) Effect of erythromycin exposure on the growth, antioxidante system and photosynthesisof Microcystis flos-aquae. J Hazard Mater 283:778–786. https://doi.org/10.1016/j.jhazmat.2014.10.026
Wang Z, Chen Q, Zhang J, Dong J, Ao Y, Wang M, Wang X (2019) Long-term exposure to antibiotic mixtures favors microcystin synthesis and release in Microcystis aeruginosa with different morphologies. Chemosphere 235:344–353. https://doi.org/10.1016/j.chemosphere.2019.06.192
Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicol Appl Pharmacol 203:201–2018. https://doi.org/10.1016/j.taap.2004.11.002
Yang W, Tang Z, Zhou F, Zhang W, Song L (2013) Toxicity studies of tetracycline on Microcystis aeruginosa and Selenastrum capricornutum. Environ. Toxicol Phar 35:320–324. https://doi.org/10.1016/j.etap.2013.01.006
Zhang T, He J, Luo X (2017) Effect of Fe and EDTA on freshwater cyanobacteria bloom formation. Water 9:326. https://doi.org/10.3390/w9050326
Zorita S, Mårtensson L, Mathiasson L (2009) Occurrence and removal of pharmaceuticals in a municipal sewage treatment system in the south of Sweden. Sci Total Environ 407:2760–2770. https://doi.org/10.1016/j.scitotenv.2008.12.030
Funding
Authors thank to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)- (n° 430383/2018-5), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)- Finance Code 001, Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Departamento de Inovação da Universidade do Estado do Rio de Janeiro (InovUerj) for the financial support received.
Author information
Authors and Affiliations
Contributions
RDSC: conceptualized the article and drafted the manuscript and literature search. GRQ: drafted the manuscript, literature search, and data analysis. HDSO: drafted the manuscript and literature search. VSDA: correction and critical review of the manuscript. JAN: writing – original draft, correction and critical review of the manuscript, and research coordinator. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable
Consent for publication
Not applicable
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Robert Duran
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(XLSX 53 kb)
Rights and permissions
About this article
Cite this article
dos Santos Costa, R., Quadra, G.R., de Oliveira Souza, H. et al. The link between pharmaceuticals and cyanobacteria: a review regarding ecotoxicological, ecological, and sanitary aspects. Environ Sci Pollut Res 28, 41638–41650 (2021). https://doi.org/10.1007/s11356-021-14698-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-14698-5