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Chronic levels of ibuprofen induces haematoxic and histopathology damage in the gills, liver, and kidney of the African sharptooth catfish (Clarias gariepinus)

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Abstract

Numerous active pharmaceutical ingredients (APIs) have been detected in various environmental matrices. Thus, their potential to elicit their toxic effect on non-target organisms is a growing concern, especially in the aquatic environment. This study aimed to investigate the potential toxicity of ibuprofen (IBU) at environmentally relevant concentration on the haematology and histology of the gill, liver, and kidney over 30 days. The 96-h acute toxicity data showed that IBU was moderately toxic to C. gariepinus with an LC50 value of 3.78 mg/L. After 15 and 30 days of exposure, there was a significant alteration in haematological indices in the treated fishes when compared to the control group. Throughout the experimental duration, the level of the mean corpuscular volume (MCV) and mean corpuscular haemoglobin (MCH) were consistently lower significantly, in contrast to the control group. IBU induced histopathological deformities in the gills, liver, and kidney of the exposed fishes, with alterations such as showing severe secondary lamella necrosis (SLN), epithelial lifting (EL), mild deformity of the secondary lamella (DSL), mild secondary lamella necrosis (MLN), and mild vascular congestion in the liver and kidney, respectively. This study has demonstrated that IBU at environmentally relevant concentrations can significantly impact the haematology, gills, liver, and kidney of C. gariepinus. This study’s results can provide baseline info for regulatory agencies to set safe limits for NSAIDs as a safeguard for the aquatic environment.

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References

  • Adamu KM, Audu BS (2008) Haematological assessment of the Nile tilapia Oreochromis niloticus exposed to sublethal concentrations of portland cement powder in solution. Int J Zool Res 4(1):48–52

    Google Scholar 

  • Adewumi AA, Olaleye VF (2011) Catfish culture in Nigeria: progress, prospects and problems. Afr J Agric Res 6(6):1281–1285

    Google Scholar 

  • Adewumi B, Ogunwole GA, Akingunsola E, Falope OC (2018) Effects of sub-lethal toxicity of chlorpyrifos and DDforce pesticides on haematological parameters of Clarias gariepinus. Int J Environ Res Public Health 5(5):62–71

    Google Scholar 

  • Aghamirkarimi S, Mashinchian AM, Sharifpour I, Jamili S, Ghavam PM (2017) Sublethal effects of copper nanoparticles on the histology of gill, liver and kidney of the Caspian roach, Rutilus rutilus caspicus. Gjesm 3(3):323–332

  • Akinrotimi OA, Agokei EO, Aranyo AA (2012) Changes in blood parameters of Tilapia guineensis exposed to different salinity levels. J Environ Eng-Asce 1(2)

  • Alaa EHS, Imam AM, Usama MM (2012) Histopathological Alterations in some Body Organs of Adult Clarias gariepinus (Burchell, 1822) Exposed to 4- Nonylphenol, Zoology, Maria-Dolores Garcia. IntechOpen. https://doi.org/10.5772/29544

  • Aliakbar H (2012) Effect of marine mercury toxicity on immunological responses of seabream. Asian Australas J Anim Sci 6:1–12

    Google Scholar 

  • Anderson HL, Brodsky IE, Mangalmurti NS (2018) The evolving erythrocyte: red blood cells as modulators of innate immunity. J Immunol Res 201:1343–1351

    CAS  Google Scholar 

  • Arun K, Archana G (2015) Haematological studies of some edible fresh water fishes of NCR region. Int J Pharm Pharm Sci 4(6):1467–1479

    Google Scholar 

  • Avwioro OG (2014) Histochemistry and tissue pathology principles and techniques, 3rd edn. Claverianum press, Nigeria ltd, p 119

    Google Scholar 

  • Awofisayo OS, Awofisayo OA, Iferi II, Akpan OE (2008) The pattern of Sale and use of non-steroidal anti- inflammatory drugs in rural and urban centres in Nigeria. Trop J Pharm Res 3:1013–1018

    Google Scholar 

  • Bartoskova M, Radka D, Vlasta S, Dana Z, Jana B, Petr M, Lenka Z, Milan B, Francesca C, Caterina F (2013) Evaluation of ibuprofen toxicity for zebrafish (Danio rerio) targeting on selected biomarkers of oxidative stress. Neuro Endocrinol 34(Suppl.2):102–108

    CAS  Google Scholar 

  • Baskar T (2014) Impact of nitrite toxicity on histopathological profile to freshwater fish, Cirrhinus Mrigala. Int J Eng Sci Technol 3(4):42–47

    Google Scholar 

  • Binukumari S, Anbalagan M, Vasanthi J (2013) A study on the effect of an insecticide encounter (herbal plant extract) on the haematology of the freshwater fish, Labeo rohita. Int J Pharm Biol Sci 8:92–94

    Google Scholar 

  • Blaxhall PC, Daisley KW (1973) Routine haematological methods for use with fish blood. J Fish Biol 5:771–781

    Google Scholar 

  • Bob-Manuel KNO, Green AF (2019) Sublethal effects of Gammalin 20® (lindane) on the haematology of Clarias gariepinus (Burchell, 1822) juveniles. Afric J Environ Nat Sci Res 2(1):46–54

    Google Scholar 

  • 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

    Google Scholar 

  • Burgos-Aceves MA, Lillà L, Caterina F (2019) Multidisciplinary haematology as prognostic device in environmental and xenobiotic stress-induced response in fish. Sci Total Environ 670:1170–1183

    CAS  Google Scholar 

  • Camargo MMP, Martinez CBR (2007) Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream. Neotrop Ichthyol 5(3):327–336. https://doi.org/10.1590/S1679-62252007000300013

  • Chaudhry HS, Kasarla MR (2019) Microcytic hypochromic anemia. [Updated 2019 Mar 2]. In: StatPearls [Internet]. StatPearls Publishing, Treasure Island 2019 Jan-. Available from: www.ncbi.nlm.nih.gov/books/NBK470252/

    Google Scholar 

  • Coles EH (1986) Veterinary clinical pathology, 4th edn. W.B. Saunder’s Company, London

    Google Scholar 

  • Corcoran J, Winter MJ, Tyler CR (2010) Pharmaceuticals in the aquatic environment: a critical review of the evidence for health effects in fish. Crit Rev Toxicol 40(4):287–304. https://doi.org/10.3109/10408440903373590

    Article  CAS  Google Scholar 

  • Dacie JV, Lewis SN (1991) Practical Haematology. Churchill, Edinburg

    Google Scholar 

  • Dacie JV, Lewis SM (2011) Practical Haematology. Churchill Livingstone, New York

    Google Scholar 

  • Davies AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22(5):760–772. https://doi.org/10.1111/j.1365-2435.2008.01467.x

  • De Moraes FD, de Figueiredo JSL, Rossi PA, Venturini FP, Moraes G (2015) Acute toxicity and sublethal effects of phenol on hematological parameters of channel catfish Ictalurus punctatus and pacu Piaractus mesopotamicus. Ecotoxicol Environ Contam 10(1):31–36

    Google Scholar 

  • El-Murr AE, Imam TS, Hakim Y, Ghonimi WAM (2015) Histopathological, immunological, hematological and biochemical effects of fipronil on Nile tilapia (Oreochromis niloticus). J Vet Sci Tech 6:5

    Google Scholar 

  • Fazio F, Marafioti S, Sanfilippo M, Casella S, Piccione G (2016) Assessment of immune blood cells and serum protein levels in Mugil cephalus (Linnaeus, 1758), Sparus aurata (Linnaeus, 1758) and Dicentrarchus labrax (Linnaeus, 1758) collected from the Thyrrhenian Sea coast (Italy). Cah Biol Mar 57:235–240

    Google Scholar 

  • Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat 76:122–159

  • Ferrando-Climent L, Collado N, Buttiglieri G, Gros M, Rodriguez-Roda I, Rodriguez-Mozaz S, Barceló D (2012) Comprehensive study of ibuprofen and its metabolites in activated sludge batch experiments and aquatic environment. Sci Total Environ 438:404–413

    CAS  Google Scholar 

  • Finney GJ (1971) Probit analysis, 3rd edn. Cambridge press, London, p 318

    Google Scholar 

  • Fraisal ASR (2003) Adverse effects of some antimicrobial agents used in fish. PhD thesis, Faculty of Veterinary Medicine, Cairo University, Cairo

  • Francesco P, Mathieu P, Senechal D (2012) Conformal field theory. Springer Science & Business Media, Berlin

    Google Scholar 

  • Gardner GR, Yevich PP (1970) Histological and hematological responses of an estuarine teleost to cadmium. J Fish Res Boa Can 27:2185–2196

    CAS  Google Scholar 

  • Han S, Choi K, Kim J, Ji K, Kim S, Aho B, Yun J, Choi K, Khim JS, Zhang X, Giesy JP (2010) Endocrine disruption and consequences of chronic exposure to ibuprofen in Japanese medaka Oryzias latipes and freshwater cladocerans Daphnia magna and Moina macrocopa. Aquat Toxicol 98:256–264. https://doi.org/10.1016/j.aquatox.2010.02.013

    Article  CAS  Google Scholar 

  • Hashemi R, Majidi A, Motamed H, Amini A, Najari F, Tabatabaey A (2015) Erythrocyte sedimentation rate measurement using as a rapid alternative to the Westergren method. Emergency (Tehran, Iran) 3(2):50–53

    Google Scholar 

  • IMS Health (2020) www.imshealth.com. Available at: http://us.imshealth.com/canada/Trends14_En_09.pdf.

  • Kasherwani D, Lodhi HS, Tiwari KJ, Shukla S, Sharma UD (2009) Cadmium toxicity to freshwater catfish, Heteropneustes fossilis (Bloch). Asian J Exp Sci 23(1):149–156

    CAS  Google Scholar 

  • Kasprzyk-Hordern B, Dinsdale RM, Guwy AJ (2008) The occurrence of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs in surface waters in South Wales, UK. Water Res 42:3498–3518

    CAS  Google Scholar 

  • Kumar R, Banerjee TK (2016) Arsenic induced hematological and biochemical responses in nutritionally important catfish Clarias batrachus (L.). Toxicol Rep 3:148–152

    CAS  Google Scholar 

  • Lan SM, Amaeze NH, Obanya HE, Okoroafor CU (2019) Occurrence of selected pharmaceuticals in industrial wastewater, receiving waters and fish. Afr J Aquat Sci 44(4):401–408

    CAS  Google Scholar 

  • Li ZH, Li P, Randak T (2011) Evaluating the toxicity of environmental concentrations of waterborne chromium (VI) to a model teleost, Oncorhynchus mykiss: a comparative study of in vivo and in vitro. Comp Biochem Physiol C 153(4):402–407

    Google Scholar 

  • Loos R, Gawlik BM, Locoro G, Rimaviciute E, Contini S, Bidoglio G (2009) EU-wide survey of polar organic persistent pollutants in European river waters. Environ Pollut 157:561–568

    CAS  Google Scholar 

  • Maharajan A, Rufus MK, Paruruckumani PS, Ganapiriya V (2016) Histopathology biomarker responses in Asian sea bass, Lates calcarifer (Bloch) exposed to copper. J Basic Appl Zool 77:21–30

    CAS  Google Scholar 

  • Marchlewicz A, Guzik U, Wojcieszyńska D (2015) Over-the-counter monocyclic non-steroidal anti-inflammatory drugs in the environment sources, risks, biodegradation. Water Air Soil Pollut 226:335

  • Martins ML, Tavares-Dias M, Fujimoto RY, Onaka EM, Nomura DT (2004) Haematological alterations of Leporinus macrocephalus (Osteichthyes: Anostomidae) naturally infected by Goezia leporini (Nematoda: Anisakidae) in fish pond. Arq Bras Med Vet Zootec 56:640–646

    Google Scholar 

  • Martins ML, Xu DH, Shoemaker CA, Klesius PH (2011) Temperature effects on immune response and hematological parameters of channel catfish Ictalurus punctatus vaccinated with live theronts of Ichthyophthirius multifiliis. Fish Shellfish Immun 31:774–780

    CAS  Google Scholar 

  • Mazon AF, Monteiro EAS, Pinheiro GHD, Fernandes MN (2002) Hematological and physiological changes induced by short-term exposure to copper in the freshwater fish Prochilodus scrofa. Braz J Biol 62(4A):621–631

    CAS  Google Scholar 

  • Medline Plus (2020) Erythrocyte Sedimentation Rate. Available at: www.medlineplus.gov/lab-tests/erythrocyte-sedimentation-rate-esr/. Accessed 26 Feb 2020

  • Mirale JB (1982) Laboratory medicine haematological, 6th edn. The CV Mosby Publishing, London, p 883

    Google Scholar 

  • Mostakim GM, Zahangir MM, Mishu MM, Rahman MK, Islam MS (2015) Alteration of blood parameters and histoarchitecture of liver and kidney of silver barb after chronic exposure to quinalphos. Int J Toxicol:415984

  • Nwani CD, Mkpadobi BN, Onyishi G, Echi PC, Chukwuka CO, Oluah SN, Njoku I (2013) Changes in behavior and hematological parameters of freshwater African catfish Clarias gariepinus (Burchell 1822) following sublethal exposure to chloramphenicol. Drug Chem Toxicol Early Online:1–7

  • Ogueji EO, Nwani CD, Iheanacho SC, Mbah CE, Okeke CO, Yaji A (2018) Acute toxicity effects of ibuprofen on behaviour and haematological parameters of African catfish Clarias gariepinus (Burchell, 1822). Afr J Aquat Sci 43(3):293–303

    CAS  Google Scholar 

  • Ogunwole GA, Saliu JK (2020) Seasonal Occurrence Of Ibuprofen In Sediment, Water, and Biota In River Owena and Ogbese, and Its Ecological Risk Assessment. Ann Sci Tech - B 5(1):11–19

  • Oliveira TZ, Andre LV, Gisela GC, Aline H, Roberto MN, Antonio O (2016) Effects of iodized salt on the histopathology of the gills and liver in Rhamdia quelen and Metynnis maculatus. Aquac Res 48(5):2198–2208

    Google Scholar 

  • Olufayo MO (2009) Haematological characteristics of Clarias gariepinus (Burchell 1822) juveniles exposed to Derris Elliptica root powder. Afr J Food Agric Nutr Dev 9(3)

  • Organisation for Economic Co-operation and Development (2010) Short guidance on the threshold approach for acute fish toxicity testing. series on testing and assessment. No. 126. www.oecd.org.

  • Parolini M, Binelli A, Provini A (2011) Chronic effects induced by ibuprofen on the freshwater bivalve Dreissena polymorpha. Ecotox Environ Safe 74:1586–1594

    CAS  Google Scholar 

  • Parrino V, Cappello T, Costa G, Cannavà C, Sanfilippo M, Fazio F, Fasulo S (2018) Comparative study of haematology of two teleost fish (Mugil cephalus and Carassius auratus) from different environments and feeding habits. Eur Zool J 85(1):193–199

    Google Scholar 

  • Pereira S, Pinto AL, Cortes R, Fontaınhas-Fernandes A, Coimbra AM, Monteiro SM (2013) Gill histopathological and oxidative stress evaluation in native fish captured in Portuguese northwestern rivers. Ecotox Environ Safe 90:157–166

    CAS  Google Scholar 

  • Rabitto IS, Alves Costa JR, Silva de Assis HC, Pelletier EE, Akaishi FM, Anjos A, Randi MA, Oliveira Ribeiro CA (2005) Effects of dietary Pb (II) and tributyltin on neotropical fish, Hoplias malabaricus: Histopathological and biochemical findings. Ecotoxicol Environ Saf 60:147–156

    CAS  Google Scholar 

  • Sakr SA, Al J, Lail SM (2005) Fenvalerate induced histopathological and histochemical changes in the liver of the cat fish Clarias gariepinus. Res J Appl Sci 1(3):263–267

    Google Scholar 

  • Samuel VK, Little FP, Samuel T, Muniyasamy P, Kalyanasundaram D, Deepa P, Rajasingh R, Subramanian A, Mohamed M (2018) Haematological studies of Anabas testudineus Bloch 1792 on exposure to aquatic toxicants of Buckingham canal, Chennai, Tamil Nadu. India Int J Fish Aquat Stud 6(4):55–59

    Google Scholar 

  • Saravanan M, Devi KU, Malarvizhi A, Ramesh M (2012) Effects of ibuprofen on hematological, biochemical and enzymological parameters of blood in an Indian major carp, Cirrhinus mrigala. Environ Toxicol Pharmacol 34:14–22. https://doi.org/10.1016/j.etap.2012.02.005

    Article  CAS  Google Scholar 

  • Sayed AEH, Moneeb RH (2015) Hematological and biochemical characters of monosex tilapia (Oreochromis niloticus, Linnaeus, 1758) cultivated using methyltestosterone. Jobaz 72:36–42

  • Sayed AEH, Mekkawy IA, Mahmoud UM (2012) Histopathological alterations in some body organs of adult Clarias gariepinus (Burchell, 1822) exposed to 4-nonylphenol. IntechOpen Zool 8:163–184

    Google Scholar 

  • Strzyżewska-Worotyńska E, Szarek J, Babińska I, Gulda D (2017) Gills as morphological biomarkers in extensive and intensive rainbow trout (Oncorhynchus mykiss, Walbaum 1792) production technologies. Environ Monit Assess 189:611. https://doi.org/10.1007/s10661-017-6278-7

    Article  CAS  Google Scholar 

  • Summit Medical Group (2020) Erythrocyte Sedimentation Rate Test. Available at: www.summitmedicalgroup.com/library/adult_health/aha_esr_test/. Accessed 26 Feb 2020

  • Thophon S, Kruatrachue M, Upathan ES, Pokethitiyook P, Sahaphong S, Jarikhuan S (2003) Histopathological alterations of white seabass, Lates calcarifer in acute and subchronic cadmium exposure. Environ Pollut 121:307–320

  • Tincey V (2017) Enhancing aquatic hypoxia: responses, adaptability and mitigation measures. Green Challenges Newsletter, Mumbai

    Google Scholar 

  • Umamaheswari S, Senthilnathan S (2013) Effect of diethylphthalate on the haematological parameters of the freshwater fish Oreochromis mossambicus (Tilapia). Eur Zool J 2(4):55–59

    Google Scholar 

  • USEPA (2009) Origins and fate of PPCPs in the environment; http://www.epa.gov/ppcp/pdf/drawing.pdf; As posted on August 20, 2009. USEPA Office of Research and Development, National Exposure Research Laboratory

  • Wedemeyer CA, Yasutake WT (1983) Clinical methods for the assessment of the effects of environmental stress on fish health. In: United States Technical Papers and United States Fish Wildlife Services, vol 89, pp 1–18

    Google Scholar 

  • Williams RT, Cook JC (2007) Exposure to pharmaceuticals present in the environment. Drug Inform J 41:133–141

    Google Scholar 

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Acknowledgements

We wish to thank the Laboratory for Interdisciplinary Statistical Analysis (LISA), of the Federal University of Technology, Akure, for their immense statistical tutoring and guidance that facilitated the validity of this study.

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Germaine Akinola Ogunwole and Joseph Kayode Saliu designed and conceptualized the experiment, Joseph Kayode Saliu and Fidelia Ijeoma Osuala supervised the experimental procedures, and Germaine Akinola Ogunwole and Faith Oluwaseyi Odunjo undertook the experiment. The statistical analysis and manuscript writing was done by Germaine Akinola Ogunwole, and the manuscript was proofread by Joseph Kayode Saliu. All authors read and approved the final manuscript.

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Correspondence to Germaine Akinola Ogunwole.

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All experimental procedures were approved by the institutional ethics clearance committee with reference number CERAD/REC/10/19/011 and performed in compliance with the standards described by the institution of animal welfare act in line with the National Environmental Standard Regulations Enforcement Agency (NESREA) Act of Nigeria on the protection of animals against cruelty.

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Ogunwole, G.A., Saliu, J.K., Osuala, F.I. et al. Chronic levels of ibuprofen induces haematoxic and histopathology damage in the gills, liver, and kidney of the African sharptooth catfish (Clarias gariepinus). Environ Sci Pollut Res 28, 25603–25613 (2021). https://doi.org/10.1007/s11356-020-12286-7

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