{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,21]],"date-time":"2026-05-21T00:31:54Z","timestamp":1779323514379,"version":"3.51.4"},"reference-count":96,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2025,5,14]],"date-time":"2025-05-14T00:00:00Z","timestamp":1747180800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ecology, Biology, and Physiology of Aquatic Organisms Laboratory, Faculty of Sciences, University of Tunis El Manar, and the Centre Technique d\u2019Aquaculture (CTA), Ministry of Agriculture, Hydraulic Resources and Fisheries","award":["RSP2025R17"],"award-info":[{"award-number":["RSP2025R17"]}]},{"DOI":"10.13039\/501100002383","name":"King Saud University","doi-asserted-by":"publisher","award":["RSP2025R17"],"award-info":[{"award-number":["RSP2025R17"]}],"id":[{"id":"10.13039\/501100002383","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Microplastics (MPs) are contaminants of emerging concern, and the study of their effects on several species, especially freshwater organisms, has not been exhausted. Erpobdella johanssoni, a freshwater leech, was used as a model in this study for the assessment of the potentially toxic effects of polyethylene microplastics (PE-MPs) 40\u201348 \u00b5m in size under controlled laboratory conditions. PE-MP toxicity was assessed in the examined leech using four increasing concentrations (1, 10, 100, and 1000 \u00b5g\/L) during an exposure period of 7 days. Oxidative damage was detected through the increase in malondialdehyde (MDA) levels, reflecting the occurrence of lipid peroxidation. The activities of enzymes involved in the antioxidant response, such as catalase (CAT), superoxide dismutase (SOD), and glutathione peroxidase (GPx), increased. Furthermore, the histopathology of the body wall, muscle cells, botryoidal cells, and ovaries was assessed to understand and evaluate the acute toxicity of PE-MPs. The histopathological changes detected in PE-MP-treated leeches varied in a concentration-dependent manner. Overall, this research indicated that even at environmentally relevant concentrations, PE-MPs had biological effects on the studied leeches and, consequently, on the freshwater invertebrate clade. This finding could provide novel insights into the effects of plastic pollution on freshwater ecosystems, particularly on invertebrate health and biodiversity.<\/jats:p>","DOI":"10.3390\/ani15101417","type":"journal-article","created":{"date-parts":[[2025,5,14]],"date-time":"2025-05-14T08:44:58Z","timestamp":1747212298000},"page":"1417","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Assessing the Effect of Polyethylene Microplastics in the Freshwater Leech Erpobdella johanssoni (Annelida, Hirudinida) Through Integrated Biomarkers and Histopathological Analysis"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0880-2855","authenticated-orcid":false,"given":"Raja","family":"Ben Ahmed","sequence":"first","affiliation":[{"name":"Ecology, Biology and Physiology of Aquatic Organisms Laboratory, Department of Biology, Faculty of Sciences of Tunis, University of Tunis El Manar, Tunis 2092, Tunisia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-8342-854X","authenticated-orcid":false,"given":"Ichrak","family":"Khaled","sequence":"additional","affiliation":[{"name":"Laboratory of Biotechnology and Biomonitoring of the Environment and Oasis Ecosystems (LBBEEO), Faculty of Sciences of Gafsa, University of Gafsa, Gafsa 2112, Tunisia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2631-2099","authenticated-orcid":false,"given":"Tahani","family":"El Ayari","sequence":"additional","affiliation":[{"name":"Group of Fundamental and Applied Malacology (LEB\/GFAM), Laboratory of Environment Biomonitoring, Faculty of Sciences of Bizerte, University of Carthage, 7021 Zarzouna, Bizerte 1054, Tunisia"},{"name":"Faculty of Sciences of Gafsa, University of Gafsa, Gafsa 2112, Tunisia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5400-6705","authenticated-orcid":false,"given":"Issam","family":"Saidi","sequence":"additional","affiliation":[{"name":"Laboratory of Biotechnology and Biomonitoring of the Environment and Oasis Ecosystems (LBBEEO), Faculty of Sciences of Gafsa, University of Gafsa, Gafsa 2112, Tunisia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2170-1303","authenticated-orcid":false,"given":"Abdel Halim","family":"Harrath","sequence":"additional","affiliation":[{"name":"Department of Zoology, College of Sciences, King Saud University, Riyadh 11451, Saudi Arabia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,5,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1743","DOI":"10.1016\/j.polymdegradstab.2007.03.029","article-title":"Biofouling and biodegradation of polyolefins in ocean waters","volume":"92","author":"Sudhakar","year":"2007","journal-title":"Polym. Degrad. Stab."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"110982","DOI":"10.1016\/j.marpolbul.2020.110982","article-title":"Quantification of microplastics using Nile Red in two bivalve species Perna viridis and Meretrix meretrix from three estuaries in Pondicherry, India and microplastic uptake by local communities through bivalve diet","volume":"153","author":"Dowarah","year":"2020","journal-title":"Mar. Pollut. Bull."},{"key":"ref_3","first-page":"100298","article-title":"New insights into the environmental behavior and ecological toxicity of microplastics","volume":"10","author":"Saud","year":"2023","journal-title":"J. Hazard. Mater. Adv."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"130146","DOI":"10.1016\/j.jhazmat.2022.130146","article-title":"Disposable face masks release microparticles to the aqueous environment after simulating sunlight aging: Microplastics or non-microplastics?","volume":"443","author":"Ma","year":"2023","journal-title":"J. Hazard. Mater."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"106430","DOI":"10.1016\/j.aquatox.2023.106430","article-title":"Polystyrene microplastics alleviate adverse effects of benzo[a]pyrene on tissues and cells of the marine mussel, Mytilus galloprovincialis","volume":"256","author":"Wang","year":"2023","journal-title":"Aquat. Toxicol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"137727","DOI":"10.1016\/j.chemosphere.2022.137727","article-title":"Microplastics pollution in freshwater sediments: The pollution status assessment and sustainable management measures","volume":"314","author":"Yin","year":"2023","journal-title":"Chemosphere"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1065","DOI":"10.1021\/acs.estlett.1c00748","article-title":"Release of microplastics from discarded surgical masks and their adverse impacts on the marine copepod Tigriopus japonicus","volume":"8","author":"Sun","year":"2021","journal-title":"Environ. Sci. Technol. Lett."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1016\/j.marpolbul.2015.07.029","article-title":"Characterisation, quantity, and sorptive properties of microplastics extracted from cosmetics","volume":"99","author":"Napper","year":"2015","journal-title":"Mar. Pollut. Bull."},{"key":"ref_9","first-page":"1022","article-title":"Policy: Classify plastic waste as hazardous","volume":"339","author":"Rochman","year":"2013","journal-title":"Science"},{"key":"ref_10","first-page":"2021","article-title":"Microplastics in the marine environment: Impacts of microplastics on aquatic organisms","volume":"34","author":"Gouin","year":"2015","journal-title":"Environ. Toxicol. Chem."},{"key":"ref_11","first-page":"24712","article-title":"Microplastic pollution and its effects on aquatic organisms","volume":"23","author":"Jemec","year":"2016","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_12","first-page":"624","article-title":"Microplastics in aquatic organisms: A review of the impacts on health and behavior","volume":"239","author":"Rist","year":"2018","journal-title":"Environ. Pollut."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"137512","DOI":"10.1016\/j.scitotenv.2020.137512","article-title":"Microplastics in the freshwater and terrestrial environments: Prevalence, fates, impacts and sustainable solutions","volume":"719","author":"Wong","year":"2020","journal-title":"Sci. Total Environ."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"114576","DOI":"10.1016\/j.envpol.2020.114576","article-title":"First report on the presence of small microplastics (\u22643 \u03bcm) in tissue of the commercial fish Serranus scriba (Linnaeus, 1758) from Tunisian coasts and associated cellular alterations","volume":"263","author":"Zitouni","year":"2020","journal-title":"Environ. Pollut."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"124055","DOI":"10.1016\/j.jhazmat.2020.124055","article-title":"Uptake, tissue distribution and toxicological effects of environmental microplastics in early juvenile fish Dicentrarchus labrax","volume":"403","author":"Zitouni","year":"2021","journal-title":"J. Hazard. Mater."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1016\/j.watres.2018.06.015","article-title":"Freshwater plastic pollution: Recognizing research biases and identifying knowledge gaps","volume":"143","author":"Blettler","year":"2018","journal-title":"Water Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.watres.2015.02.012","article-title":"Microplastics in freshwater systems: A review of the emerging threats, identification of knowledge gaps and prioritization of research needs","volume":"75","author":"Thompson","year":"2015","journal-title":"Water Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1016\/j.scitotenv.2018.07.207","article-title":"Studies of the effects of microplastics on aquatic organisms: What do we know and where should we focus our efforts in the future?","volume":"645","author":"Oliveira","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_19","first-page":"118679","article-title":"Microplastic pollution in freshwater systems: A review of contamination sources, accumulation, and impacts on aquatic biota","volume":"295","author":"Smith","year":"2022","journal-title":"Environ. Pollut."},{"key":"ref_20","first-page":"159545","article-title":"Assessing microplastic distribution and ecological risks in riverine environments","volume":"857","author":"Johnson","year":"2023","journal-title":"Sci. Total Environ."},{"key":"ref_21","first-page":"65","article-title":"Quantity and type of plastic debris flowing from two urban rivers to coastal waters and beaches of Southern California","volume":"11","author":"Moore","year":"2011","journal-title":"Rev. Gest\u00e3o Costeira Integr. J. Integr. Coast. Zone Manag."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1111\/gwat.12862","article-title":"Microplastic contamination in karst groundwater systems","volume":"57","author":"Panno","year":"2019","journal-title":"Groundwater"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"124844","DOI":"10.1016\/j.jhazmat.2020.124844","article-title":"Experimental field evidence for transport of microplastic tracers over large distances in an alluvial aquifer","volume":"408","author":"Goeppert","year":"2021","journal-title":"J. Hazard. Mater."},{"key":"ref_24","first-page":"265","article-title":"First evaluation of microplastics in surface and deep sediments of the southern Mediterranean Sea: The case of Tunisia","volume":"136","author":"Toumi","year":"2019","journal-title":"Mar. Pollut. Bull."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"161027","DOI":"10.1016\/j.scitotenv.2022.161027","article-title":"Microplastics contamination and characteristics of agricultural groundwater in Haean Basin of Korea","volume":"864","author":"Cha","year":"2023","journal-title":"Sci. Total Environ."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"161578","DOI":"10.1016\/j.scitotenv.2023.161578","article-title":"Spatial distribution characteristics and migration of microplastics in surface water, groundwater and sediment in karst areas: The case of Yulong River in Guilin, Southwest China","volume":"868","author":"Shu","year":"2023","journal-title":"Sci. Total Environ."},{"key":"ref_27","first-page":"13499","article-title":"Microplastics in commercial molluscs from Tunisia: Assessment of the contamination and effect of digestive processes","volume":"24","author":"Abidli","year":"2017","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"14673","DOI":"10.1007\/s11356-019-04695-0","article-title":"Microplastics in freshwater environment: The first evaluation in sediments from seven water streams surrounding the lagoon of Bizerte (Northern Tunisia)","volume":"26","author":"Toumi","year":"2019","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_29","first-page":"1","article-title":"Microplastics in sediments of the River Thames Basin, UK\u2014Abundance, sources and methods for effective quantification","volume":"113","author":"Fischer","year":"2016","journal-title":"Mar. Pollut. Bull."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1596","DOI":"10.1016\/j.marpolbul.2011.05.030","article-title":"Microplastics in the marine environment","volume":"62","author":"Andrady","year":"2011","journal-title":"Mar. Pollut. Bull."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/s12302-014-0012-7","article-title":"Microplastics in freshwater ecosystems: What we know and what we need to know","volume":"26","author":"Wagner","year":"2014","journal-title":"Environ. Sci. Eur."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.trac.2018.12.001","article-title":"Ecotoxicological effects of microplastics: Examination of biomarkers, current state and future perspectives","volume":"111","author":"Faggio","year":"2019","journal-title":"TrAC Trends Anal. Chem."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.chemosphere.2018.09.032","article-title":"Marine microplastic: Preparation of relevant test materials for laboratory assessment of ecosystem impacts","volume":"213","author":"Booth","year":"2018","journal-title":"Chemosphere"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/j.marpolbul.2019.03.048","article-title":"Microplastics in commercial molluscs from the lagoon of Bizerte (Northern Tunisia)","volume":"142","author":"Abidli","year":"2019","journal-title":"Mar. Pollut. Bull."},{"key":"ref_35","first-page":"2843","article-title":"Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L.)","volume":"45","author":"Browne","year":"2011","journal-title":"Environ. Sci. Technol."},{"key":"ref_36","first-page":"101581","article-title":"First evaluation of microplastics in two commercial fish species from the lagoons of Bizerte and Ghar El Melh (Northern Tunisia)","volume":"41","author":"Abidli","year":"2021","journal-title":"Reg. Stud. Mar. Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.marpolbul.2012.11.028","article-title":"Occurrence of microplastics in the gastrointestinal tract of pelagic and demersal fish from the English Channel","volume":"67","author":"Lusher","year":"2013","journal-title":"Mar. Pollut. Bull."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1007\/s002449900417","article-title":"Selection of an aquatic indicator species to monitor organic contaminants in trophically simple lotic food webs","volume":"35","author":"Scrimgeour","year":"1998","journal-title":"Arch. Environ. Contam. Toxicol."},{"key":"ref_39","first-page":"65","article-title":"Testing the suitability of leeches (Hirudinea, Clitellata) for biological assessment of lowland streams","volume":"53","author":"Koperski","year":"2005","journal-title":"Pol. J. Ecol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1416","DOI":"10.1016\/j.ecoenv.2011.04.001","article-title":"Assessment of genotoxic potency of sulfate-rich surface waters on medicinal leech and human leukocytes using different versions of the Comet assay","volume":"74","author":"Ternjej","year":"2011","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1080\/07924259.2016.1208118","article-title":"Effect of oil-related environmental pollutants on gonads of the freshwater leech Limnatis nilotica (Annelida, Hirudinea)","volume":"60","author":"Khaled","year":"2016","journal-title":"Invertebr. Reprod. Dev."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1807","DOI":"10.3390\/s90301807","article-title":"Leeches as sensor-bioindicators of river contamination by PCBs","volume":"9","author":"Macova","year":"2009","journal-title":"Sensors"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1080\/24750263.2017.1329360","article-title":"Impact of oil-related environmental pollutants on the ovary structure in the freshwater leech Erpobdella johanssoni (Johansson, 1927) (Clitellata: Hirudinea)","volume":"84","author":"Khaled","year":"2017","journal-title":"Eur. Zool. J."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"102196","DOI":"10.1016\/j.jksus.2022.102196","article-title":"BTEX induces histopathological alterations, oxidative stress response and DNA damage in the testis of the freshwater leech Erpobdella johanssoni (Johansson, 1927)","volume":"34","author":"Khaled","year":"2022","journal-title":"J. King Saud Univ. Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.micron.2012.07.005","article-title":"An ultrastructural study of the ovary cord organization and oogenesis in Erpobdella johanssoni (Annelida, Clitellata: Hirudinida)","volume":"44","author":"Tekaya","year":"2013","journal-title":"Micron"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Eriksen, M., Cowger, W., Erdle, L.M., Coffin, S., Villarrubia-G\u00f3mez, P., Moore, C.J., Carpenter, E.J., Day, R.H., Thiel, M., and Wilcox, C. (2023). A growing plastic smog, now estimated to be over 170 trillion plastic particles afloat in the world\u2019s oceans\u2014Urgent solutions required. PLoS ONE, 18.","DOI":"10.1371\/journal.pone.0281596"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"3471","DOI":"10.1016\/j.bbamcr.2013.06.010","article-title":"Cell death by cornification","volume":"1833","author":"Eckhart","year":"2013","journal-title":"Biochimica Biophysica Acta (BBA) Mol. Cell Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1063","DOI":"10.1111\/j.1600-0625.2008.00786.x","article-title":"The skin: An indispensable barrier","volume":"17","author":"Proksch","year":"2008","journal-title":"Exp. Dermatol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s00441-021-03549-x","article-title":"Comparison of body wall histologic structure of two medicinal leeches Hirudo sulukii and Hirudo verbana (Hirudinida: Hirudinidae)","volume":"387","year":"2022","journal-title":"Cell Tissue Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"110133","DOI":"10.1016\/j.ecoenv.2019.110133","article-title":"Exposure to polystyrene microplastics causes reproductive toxicity through oxidative stress and activation of the p38 MAPK signaling pathway","volume":"190","author":"Xie","year":"2020","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.coesh.2017.10.003","article-title":"Micro(nano)plastics: A threat to human health?","volume":"1","author":"Revel","year":"2019","journal-title":"Curr. Opin. Environ. Sci. Health"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"26643","DOI":"10.1007\/s11356-021-12506-8","article-title":"Effects of environmentally relevant levels of polyethylene microplastic on Mytilus galloprovincialis (Mollusca: Bivalvia): Filtration rate and oxidative stress","volume":"28","author":"Abidli","year":"2021","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1111\/j.1432-1033.1974.tb03751.x","article-title":"Heterogeneity of Erythrocyte Catalase II","volume":"48","author":"Aebi","year":"1974","journal-title":"Eur. J. Biochem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1016\/0003-2697(87)90489-1","article-title":"Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions","volume":"161","author":"Beyer","year":"1987","journal-title":"Anal. Biochem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1016\/S0076-6879(84)05015-1","article-title":"Assays of glutathione peroxidase","volume":"105","year":"1984","journal-title":"Methods Enzymol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/0968-0004(90)90206-Q","article-title":"The measurement and mechanism of lipid peroxidation in biological systems","volume":"15","author":"Gutteridge","year":"1990","journal-title":"Trends Biochem. Sci."},{"key":"ref_58","first-page":"e00060","article-title":"Aspidogastrea africanus Infections, comparative assessment of BTEX and heavy metals bioaccumulation, and histopathological alterations as biomarker response in Chrysichthys nigrodigitatus (Lac\u00e9p\u00e8de, 1803) of Lekki Lagoon, Nigeria","volume":"3","author":"Akinsanya","year":"2019","journal-title":"Sci. Afr."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1016\/j.chemosphere.2019.03.140","article-title":"The effects of hexaconazole and epoxiconazole enantiomers on metabolic profile following exposure to zebrafish (Danio rerio) as well as the histopathological changes","volume":"226","author":"Jia","year":"2019","journal-title":"Chemosphere"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"138821","DOI":"10.1016\/j.scitotenv.2020.138821","article-title":"Environmentally relevant concentrations of bifenthrin induce changes in behaviour, biomarkers, histological characteristics, and the transcriptome in Corbicula fluminea","volume":"728","author":"Zhang","year":"2020","journal-title":"Sci. Total Environ."},{"key":"ref_61","first-page":"1","article-title":"Studies on the histology of the body wall of two species of leeches, Erpobdella octoculata and Haemopis sanguisuga","volume":"1","author":"Ahmed","year":"2013","journal-title":"Adv. J. Biol. Sci. Res."},{"key":"ref_62","unstructured":"Khaled, I., Ahmed, R.B., Saidi, I., Pacioglu, O., and Harrath, A. (2023). Cadmium exposure induced oxidative stress and histopathological disruption in the body wall of the freshwater leech Limnatis nilotica (Savigny, 1822). Invertebr. Surv. J., 44\u201354."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"81","DOI":"10.4103\/jmau.jmau_45_22","article-title":"Light microscopy and ultrastructure of body wall in leech Haemadipsa zeylanica","volume":"11","author":"Anilkumar","year":"2023","journal-title":"J. Microsc. Ultrastruct."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.tice.2008.05.003","article-title":"Cell dynamics during cocoon secretion in the aquatic leech, Theromyzon tessulatum (Annelida: Clitellata: Glossiphoniidae)","volume":"41","author":"Sayers","year":"2009","journal-title":"Tissue Cell"},{"key":"ref_65","first-page":"1078","article-title":"Histomorphological and histochemical studies on the epidermis of the lumbricid worm, Dendrobaena atheca Cernosvitov. Z. Mikrosk.-anat","volume":"96","author":"Gorgees","year":"1982","journal-title":"Forsch."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1002\/jmor.1051770104","article-title":"The cocoon-producing cells of Eisenia foetida (Annelida, Oligochaeta): A histochemical and ultrastructural study","volume":"177","author":"Morris","year":"1983","journal-title":"J. Morphol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1016\/j.fsi.2022.06.043","article-title":"Hirudo verbana as a freshwater invertebrate model to assess the effects of polypropylene micro and nanoplastics dispersion in freshwater","volume":"127","author":"Baranzini","year":"2022","journal-title":"Fish Shellfish Immunol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"189","DOI":"10.2989\/16085914.2023.2200853","article-title":"Cadmium exposure induces testicular oxidative damage and histopathological changes in the freshwater leech Limnatis nilotica (Savigny, 1822): The protective role of salicylic acid","volume":"48","author":"Khaled","year":"2023","journal-title":"Afr. J. Aquat. Sci."},{"key":"ref_69","first-page":"1186","article-title":"Effect of copper on the body wall structures of the medicinal leech Hirudo verbana Carena, 1820","volume":"19","author":"Kutlu","year":"2010","journal-title":"Fresenius Environ. Bull."},{"key":"ref_70","first-page":"27","article-title":"Basic morphofunctional features of pharmaceutic leech (Hirudo verbana Carena, 1820) tissues in various forms of response after hirudotherapeutic procedures","volume":"61","author":"Frolov","year":"2015","journal-title":"Ann. Parasitol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4172\/2157-7439.1000323","article-title":"Cytokine impregnated biomatrix: A new tool to study multi-wall carbon nanotubes effects on invertebrate immune cells","volume":"6","author":"Girardello","year":"2015","journal-title":"J. Nanomed. Nanotechnol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Girardello, R., Tasselli, S., Baranzini, N., Valvassori, R., de Eguileor, M., and Grimaldi, A. (2015). Effects of carbon nanotube environmental dispersion on an aquatic invertebrate, Hirudo medicinalis. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0144361"},{"key":"ref_73","unstructured":"Prasad, S. (1980). Life of Invertebrates, Vikas Publishing House."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1111\/j.1525-142X.2007.00184.x","article-title":"Evolutionary aspects of pattern formation during clitellate muscle development","volume":"9","author":"Bergter","year":"2007","journal-title":"Evol. Dev."},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Kristan Jr, W.B., Skalak, R., Wilson, R.J., Skierczynski, B.A., Murray, J.A., Eisenhart, F.J., Cacciatore, T.W., Chiel, H.J., and Beer, R.D. (2000). Biomechanics of hydroskeletons: Studies of crawling in the medicinal leech. Biomechanics and Neural Control of Posture and Movement, Springer.","DOI":"10.1007\/978-1-4612-2104-3_14"},{"key":"ref_76","first-page":"475","article-title":"Water and sediment toxicity assessment by use of behavioural responses of medicinal leeches","volume":"28","year":"2003","journal-title":"Environ. Int."},{"key":"ref_77","first-page":"1","article-title":"Effects of copper sulfate exposure on the nervous system of the Hirudo verbana leech","volume":"6","author":"Cameron","year":"2023","journal-title":"Emerg. Investig."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"106538","DOI":"10.1016\/j.aquatox.2023.106538","article-title":"Single and combined effects of cadmium, microplastics, and their mixture on whole-body serotonin and feeding behaviour following chronic exposure and subsequent recovery in the freshwater leech, Nephelopsis obscura","volume":"259","author":"Zink","year":"2023","journal-title":"Aquat. Toxicol."},{"key":"ref_79","first-page":"1534","article-title":"Effects of microplastics on the freshwater leech Nephelopsis obscura: Implications for environmental health assessments","volume":"40","author":"Zink","year":"2021","journal-title":"Environ. Toxicol. Chem."},{"key":"ref_80","first-page":"431","article-title":"Erpobdellid leeches (Annelida, Clitellata, Hirudinida) from Tunisia: New records with the description of a new Trocheta species","volume":"3682","author":"Tekaya","year":"2013","journal-title":"Zootaxa"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"128161","DOI":"10.1016\/j.chemosphere.2020.128161","article-title":"Exposure to polystyrene microplastics impairs gonads of zebrafish (Danio rerio)","volume":"263","author":"Qiang","year":"2021","journal-title":"Chemosphere"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"94","DOI":"10.20473\/jafh.v12i1.36877","article-title":"Effect of Microplastic Exposures to The Male Gonad Histology of Catfish (Clarias gariepinus)","volume":"12","author":"Laily","year":"2023","journal-title":"J. Aquacult. Fish Health"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"471","DOI":"10.2983\/035.032.0227","article-title":"Gonadal state of the oyster Crassostrea angulata cultivated in Taiwan","volume":"32","author":"Vaschenko","year":"2013","journal-title":"J. Shellfish Res."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"0116","DOI":"10.1038\/s41559-017-0116","article-title":"Interactions of microplastic debris throughout the marine ecosystem","volume":"1","author":"Galloway","year":"2017","journal-title":"Nat. Ecol. Evol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"2331","DOI":"10.1073\/pnas.1600715113","article-title":"Marine microplastics spell big problems for future generations","volume":"113","author":"Galloway","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.zool.2018.08.001","article-title":"Comparative assessment of the antioxidative defense system in subadult and adult anurans: A lesson from the Bufotes viridis toad","volume":"130","author":"Faggio","year":"2018","journal-title":"Zoology"},{"key":"ref_87","first-page":"112097","article-title":"Microplastic ingestion by commercial fish from the Mediterranean Sea around Tunisia","volume":"164","author":"Abidli","year":"2021","journal-title":"Mar. Pollut. Bull."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.marenvres.2013.07.006","article-title":"Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms","volume":"93","author":"Regoli","year":"2014","journal-title":"Mar. Environ. Res."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1016\/j.aquatox.2016.10.010","article-title":"Cytotoxicity, haemolymphatic parameters, and oxidative stress following exposure to sub-lethal concentrations of quaternium-15 in Mytilus galloprovincialis","volume":"180","author":"Faggio","year":"2016","journal-title":"Aquat. Toxicol."},{"key":"ref_90","first-page":"1","article-title":"Effect of lead graded doses in Mactra corallina gills: Antioxidants status, cholinergic function and histopathological studies","volume":"5","author":"Chetoui","year":"2019","journal-title":"J. Drug Des. Med. Chem."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1147","DOI":"10.1042\/BST0351147","article-title":"Biochemistry of oxidative stress","volume":"35","author":"Halliwell","year":"2007","journal-title":"Biochem. Soc. Trans."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1098","DOI":"10.3109\/10715762.2010.498477","article-title":"Chemistry and biochemistry of lipid peroxidation products","volume":"44","author":"Atalay","year":"2010","journal-title":"Free Radic. Res."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1361","DOI":"10.1016\/j.marpolbul.2007.05.018","article-title":"Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals\u2019 pollution in coastal areas from the Saronikos Gulf of Greece","volume":"54","author":"Vlahogianni","year":"2007","journal-title":"Mar. Pollut. Bull."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"7966","DOI":"10.1002\/jcp.30468","article-title":"Oxidative stress in oocyte aging and female reproduction","volume":"236","author":"Wang","year":"2021","journal-title":"J. Cell. Physiol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"105000","DOI":"10.1016\/j.marenvres.2020.105000","article-title":"Metal body burden and tissue oxidative status in the bivalve Venerupis decussata from Tunisian coastal lagoons","volume":"159","author":"Bejaoui","year":"2020","journal-title":"Mar. Environ. Res."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1016\/j.scitotenv.2019.04.157","article-title":"Time-dependent effects of polystyrene nanoparticles in brine shrimp Artemia franciscana at physiological, biochemical and molecular levels","volume":"675","author":"Perini","year":"2019","journal-title":"Sci. Total Environ."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/15\/10\/1417\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:32:34Z","timestamp":1760031154000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/15\/10\/1417"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,14]]},"references-count":96,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["ani15101417"],"URL":"https:\/\/doi.org\/10.3390\/ani15101417","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,14]]}}}