Cookies Notification

We use cookies to improve your website experience. To learn about our use of cookies and how you can manage your cookie settings, please see our Cookie Policy.

Potential protective effects of the edible alga Arthrospira platensis against lead-induced oxidative stress, anemia, kidney injury, and histopathological changes in adult rats

Publication: Applied Physiology, Nutrition, and Metabolism
23 August 2018


Oxidative damage has been proposed as a possible mechanism involved in lead toxicity. This study investigated the possible protective effect of dietary Arthrospira platensis supplementation against lead acetate-induced kidney injury in adult male rats. Rats were divided into 4 groups: normal rats (control rats), rats treated with spirulina, rats treated with lead (Pb) (0.344 g/kg body weight), and rats treated with Pb and spirulina. The exposure of rats to Pb for 30 days provoked renal damage with significant increases in hematological parameters, oxidative stress-related parameters (i.e., thiobarbituric acid reactive substances, protein carbonyl content, advanced oxidation protein products, and hydrogen peroxide), creatinine and urea levels in plasma, and uric acid level in urine. Conversely, antioxidant enzyme activities (i.e., catalase, glutathione peroxidase, and superoxide dismutase) and levels of nonprotein thiols, plasma uric acid, and urinary creatinine and urea decreased. The administration of spirulina to Pb-treated rats significantly improved weight, peripheral blood parameters, oxidative stress-related parameters, renal biomarker levels, and antioxidant enzyme activities. Also, rats treated with Pb and spirulina had normal kidney histology. These healing effects are likely the result of the high phenol content and significant antioxidant capacity of A. platensis. Our data strongly suggest that spirulina supplementation improves kidney function and plays an important role in the prevention of complications of Pb intoxication.


Selon des études, les dommages oxydatifs constitueraient un mécanisme plausible de la toxicité du plomb. Cette étude examine chez des rats mâles adultes le possible effet protecteur de la supplémentation en Arthrospira platensis alimentaire contre les lésions au rein dues à l’acétate de plomb. On répartit les rats dans quatre groupes : normaux (contrôle), traités à la spiruline, traités au plomb (« Pb », 0,344 g/kg de masse corporelle) et traités au plomb et à la spiruline. L’exposition des rats au Pb durant 30 jours cause des dommages rénaux et une augmentation significative des paramètres hématologiques et des paramètres associés au stress oxydatif (c.-à-d. substances réactives à l’acide thiobarbiturique, teneur en protéines carbonylées, produits d’oxydation avancée des protéines et peroxyde d’hydrogène), de la concentration plasmatique de créatinine et d’urée et de l’acide urique dans l’urine. Inversement, on observe une diminution de l’activité des enzymes antioxydantes (c.-à-d. catalase, glutathion peroxydase et superoxyde dismutase) et du taux de thiols non protéiques, d’acide urique plasmatique, de créatinine urinaire et d’urée. L’administration de spiruline aux rats traités au plomb engendre une augmentation significative de la masse corporelle, des paramètres sanguins en périphérie, des paramètres associés au stress oxydatif, du taux des biomarqueurs rénaux et de l’activité des enzymes antioxydantes. De plus, les rats traités au plomb et à la spiruline présentent des reins normaux sur le plan histologique. Les effets curatifs sont vraisemblablement dus au riche contenu en phénols et à la capacité antioxydante significative de A. platensis. Nos résultats suggèrent fortement que la supplémentation en spiruline améliore les fonctions rénales en plus de jouer un important rôle dans la prévention des complications dues à l’intoxication au plomb. [Traduit par la Rédaction]

Get full access to this article

View all available purchase options and get full access to this article.


Abdel-Daim M.M. 2014. Pharmacodynamic interaction of Spirulina platensis with erythromycin in Egyptian Baladi bucks (Capra hircus). Small Rumin. Res. 120: 234–241.
Abdel-Daim M.M., Abuzead S.M., and Halawa S.M. 2013. Protective role of Spirulina platensis against acute deltamethrin-induced toxicity in rats. PLoS ONE, 8: e72991.
Abdel-Moneim A.M., El-Toweissy M.Y., Ali A.M., Awad Allah A.A., Darwish H.S., and Sadek I.A. 2015. Curcumin ameliorates lead (Pb2+)-induced hemato-biochemical alterations and renal oxidative damage in a rat model. Biol. Trace Elem. Res. 168: 206–220.
Aebi H. 1984. Catalase in vitro. Methods Enzymol. 105: 121–126.
Agency for Toxic Substances and Disease Registry (ATSDR). 2007. Toxicological Profile for Lead. U.S. Department of health and Human Services, Public Health Service, Atlanta, Ga., USA.
Ajith T.A., Nivitha V., and Usha S. 2007. Zingiber officinale Roscoe alone and in combination with alpha-tocopherol protect the kidney against cisplatin induced acute renal failure, Food. Chem. Toxicol. 45: 921–927.
Alvarenga R.R., Rodrigues P.B., Cantarelli V.S., Zangeronimo M.G., Da Silva Júnior J.W., Da Silva L.R., et al. 2011. Energy values and chemical composition of spirulina (Spirulina platensis) evaluated with broilers. Rev. Bras. Zoo. 40: 992–996.
Alvarez-Lario B. and Macarron-Vicente J. 2010. Uric acid and evolution. Rheumatology (Oxford), 49(11): 2010–2015.
Ames B.N., Cathcart R., and Schwiers E. 1981. Uric acid provides an antioxidant defense in humans against oxidant and radical caused aging and cancer: a hypothesis. Proc. Natl. Acad. Sci. U.S.A. 78: 6858–6862.
Avdagić N., Cosović E., Nakas-Ićindić E., Mornjaković Z., Zaciragić A., and Hadzović-Dzuvo A. 2008. Spirulina platensis protects against renal injury in rats with gentamicin-induced acute tubular necrosis. Bosn. J. Basic. Med. Sci. 8(4): 331–336.
Beauchamp C. and Fridovich I. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44(1): 276–287.
Bisson, M., Diderich, R., Hulot, C., Lacroix, G., Lefevre, J.P., Leveque, S., et al. 2005. Benzaldéhyde, INERIS-DRC-01-25590-01DR026, Version 2-1:1-34.
Bradley S.E., Bradley G.P., and Stéphan F. 1972. Role of structural imbalance in the pathogenesis of renal dysfunction in the hypothyroid rat. Trans. Assoc. Am. Phys. 85: 344–352.
Chen Y., Wang M., Rosen R.T., and Ho C.T. 1999. 2,2-Diphenyl-1-picrylhydrazyl radical-scavenging active components from Polygonum multiflorum thumb. J. Agric. Food Chem. 47(6): 2226–2228.
Cheng-Wu, Z., Chao-Tsi, T., and Zhen, Z.Y. 1994. The effects of polysaccharide and phycocyanin from Spirulina platensis on peripheral blood and hematopoietic system of bone marrow in mice. In Proceedings of the 2nd Asia Pacific Conference on Algal Biotechnology, National University of Singapore, p. 58.
Conterato G.M., Augusti P.R., Somacal S., Einsfeld L., Sobieski R., Torres J.R., and Emanuelli T. 2007. Effect of lead acetate on cytosolic thioredoxin reductase activity and oxidative stress parameters in rat kidneys. Basic Clin. Pharmacol. Toxicol. 101(2): 96–100.
Council of the European Communities 1986. Council Directive 86/609/EEC of 24 November 1986 on the approximation of laws, regulations and administrative provisions of the Member States regarding the protection of animals used for experimental and other scientific purposes. O. J. Eur. Comm. L358: 1–18.
Dewanto V., Wu X., Adom K.K., and Liu R.H. 2002. Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J. Agric. Food Chem. 50: 3010–3014.
D’Ischia M., Napolitano A., Manini P., and Panzella L. 2011. Secondary targets of nitrite-derived reactive nitrogen species: nitrosation/nitration pathways, antioxidant defense mechanisms and toxicological implications. Chem. Res. Toxicol. 24(12): 2071–2092.
Eldahshan O.A. and Abdel-Daim M.M. 2015. Phytochemical study, cytotoxic, analgesic, antipyretic and anti-inflammatory activities of Strychnos nux-vomica. Cytotechnology, 67(5): 831–844.
EFSA. 2013. Scientific Opinion on Lead in Food. EFSA Panel on Contaminants in the Food Chain (CONTAM). EFSA Parma Italy.
El-Demerdash F.M., Yousef M.I., Kedwany F.S., and Baghdadi H.H. 2004. Cadmium-induced changes in lipid peroxidation, blood hematology, biochemical parameters and semen quality of male rats: protective role of vitamin E and β-carotene. Food Chem. Toxicol. 42(10): 1563–1571.
Ellman G.L. 1959. Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82(1): 70–77.
Farooq S.M., Asokan D., Kalaiselvi P., Sakthivel R., and Varalakshmi P. 2004. Prophylactic role of phycocyanin: a study of oxalate mediated renal cell injury. Chem. Biol. Interact. 149(1): 1–7.
Flohe L. and Gunzler W.A. 1984. Assays of glutathione peroxidise. Methods Enzymol. 105: 114–121.
Gabe M. 1968. Histologic contributions on the endocrine pancreas of Ichthyophis glutinosus (L.) (gymnophione batrachian). Arch. Anat. Histol. Embryol. 51: 231–246.
Gargouri M., Ghorbel-Koubaa F., Bonenfant-Magné M., Magné C., Dauvergne X., Ksouri R., et al. 2012a. Spirulina or dandelion-enriched diet of mothers alleviates lead-induced damages in brain and cerebellum of newborn rats. Food Chem. Toxicol. 50(7): 2303–2310.
Gargouri M., Ben Saad H., Ben Amara I., Magné C., and El Feki A. 2016b. Spirulina exhibits hepatoprotective effects against lead induced oxidative injury in newborn rats. Cell. Mol. Biol. 62(10): 85–93.
Gargouri M., Soussi A., Akrouti A., Magné C., and El Feki A. 2018c. Ameliorative effects of spirulina platensis against lead-induced nephrotoxicity in newborn rats: modulation of oxidative stress and histopathological changes. EXCLI J. 17: 215–232.
Ghorbel F., Boujelbene M., Makni-Ayadi F., Guermazi F., Croute F., Soleilhavoup J.P., and El Feki A. 2002. Impact of lead given in drinking water on the endocrine and exocrine sexual activity in pubescent rats. Determination of an apoptotic process. C. R. Biol. 325: 927–940.
Gould K.S., Markham K.R., Smith R.H., and Goris J.J. 2000. Functional role of anthocyanins in the leaves of Quintinia serrata A. Cunn. J. Exp. Bot. 51: 1107–1115.
Harlalka G.V., Patil C.R., and Patil M.R. 2007. Protective effect of Kalanchoe pinnata pers. (Crassulaceae) on gentamicin-induced nephrotoxicity in rats. Ind. J. Pharmacol. 39(4): 201–205.
Hermansky S.J., Stohs S.J., Markin R.S., and Murray W.J. 2015. Hepatic lipid peroxidation, sulfhydryl status, and toxicity of the blue-green algal toxin microcystin-LR in mice. J. Toxicol. Environ. Health, 31: 71–91.
Ibrahim N.M., Eweis E.A., El-Beltagi H.S., and Abdel-Mobdy Y.E. 2012. Effect of lead acetate toxicity on experimental male albino rat. Asian Pac. J. Trop. Biomed. 2(1): 41–46.
Janicka M., Binkowski Ł.J., Błaszczyk M., Paluch J., Wojtaś W., Massanyi P., and Stawarz R. 2015. Cadmium, lead and mercury concentrations and their influence on morphological parameters in blood donors from different age groups from southern Poland. J. Trace Elem. Med. Biol. 29: 342–346.
Jollow D.J., Mitchell J.R., Zampaglione N., and Gillette J.R. 1974. Bromobenzene-induced liver necrosis: protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology, 11(3): 151–169.
Jorissen A., Plum L.M., Rink L., and Haase H. 2013. Impact of lead and mercuric ions on the interleukin-2-dependent proliferation and survival of T cells. Arch. Toxicol. 87(2): 249–258.
Koleva I.I., van Beek T.A., Linssen J.P., de Groot A., and Evstatieva L.N. 2002. Screening of plant extracts for antioxidant activity: a comparative study on three testing methods. Phytochem. Anal. 13: 8–17.
Lakshmi B.V., Sudhakar M., and Aparna M. 2013. Protective potential of Black grapes against lead induced oxidative stress in rats. Environ. Toxicol. Pharmacol. 35(3): 361–368.
Lee, G.R., Foerster, J., and Athens, J.W. 1998. Wintrobe’s clinical hematology. 10th ed. Lippincott Williams & Wilkins, New York, USA. pp. 1862–1888.
Lim S.S., Vos T., Flaxman A.D., Danaei G., Shibuya K., Adair-Rohani H., et al. 2012. A comparative risk assessment of burden of disease and injury attributable to 67risk factors and risk factor clusters in 21 regions, 1990–2010: a systematic analysis for the global burden of disease study 2010. Lancet, 380: 2224–2260.
Lowry O.H., Rosebrugh N., Farr A.L., and Randall R.J. 1951. Protein measurement with folin phenol. J Biol. Chem. 193: 265–275.
Marouane W., Soussi A., Murat J.C., Bezzine S., and El Feki A. 2011. The protective effect of Malva sylvestris on rat kidney damaged by vanadium. Lipids Health Dis. 10: 65–73.
Mohan I.K., Khan M., Shobha J.C., Naidu M.U., Prayag A., Kuppusamy P., and Kutala V.K. 2006. Protection against cisplatin-induced nephrotoxicity by Spirulina in rats. Cancer Chemother. Pharmacol. 58(6): 802–808.
Nascimento C.R.B. and Martinez C.B.R. 2016. Daily intake of lead in Wistar rats at different ages: biochemical, genotoxic and physiological effects. Environ. Toxicol. Pharmacol. 41: 132–141.
Navarro-Moreno L.G., Quintanar-Escorza M.A., González S., Mondragón R., Cerbón-Solorzáno J., Valdés J., and Calderón-Salinas J.V. 2009. Effects of lead intoxication on intercellular junctions and biochemical alterations of the renal proximal tubule cells. Toxicol. In Vitro, 23(7): 1298–1304.
Ou P. and Wolff S.P. 1996. A discontinuous method for catalase determination at near physiological concentrations of H2O2 and its application to the study of H2O2 fluxes within cells. J. Biochem. Biophys. Methods, 31: 59–67.
Oyaizu M. 1986. Studies on products of the browning reaction prepared from glucosamine. Jpn. J. Nutr. 44: 307–315.
Prieto P., Pineda M., and Aguilar M. 1999. Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal. Biochem. 269(2): 337–341.
Re R., Pellegrini N., Proteggente A., Pannala A., Yang M., and Rice-Evans C. 1999. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 26(9–10): 1231–1237.
Reznick A.Z. and Packer L. 1994. Oxidative damage to proteins: spectrophotometric method for carbonyl. Methods Enzymol. 233: 357–363.
Rhodes, C., Stryer, L., and Tasker, R. 1995. Biochemistry. 4th ed. W.H. Freeman, San Francisco, Calif. pp. 280–297.
Shah M.D. and Iqbal M. 2010. Diazinon-induced oxidative stress and renal dysfunction in rats. Food Chem. Toxicol. 48(12): 3345–3353.
Sharma S. and Singh B. 2014. Effects of acute and chronic lead exposure on kidney lipid peroxidation and antioxidant enzyme activities in BALB-C mice (Mus musculus). Int. J. Sci. Res. 3(9): 1564–1566.
Shastri D., Kumar M., and Kumar A. 1999. Modulations of lead toxicity by Spirulina fusiformis. Phytother. Res. 13: 258–260.
Simsek N., Karadeniz A., Kalkan Y., Keles O.N., and Unal B. 2009. Spirulina platensis feeding inhibited the anemia- and leucopenia-induced lead and cadmium in rats. J. Hazard. Mater. 164: 1304–1309.
Singh Z., Chadha P., and Sharma S. 2013. Evaluation of oxidative stress and genotoxicity in battery manufacturing workers occupationally exposed to lead. Toxicol. Int. 20(1): 95–100.
Soussi A., Gargouri M., and El Feki A. 2018. Effects of co-exposure to lead and zinc on redox status, kidney variables, and histopathology in adult albinos rats. Toxicol. Ind. Health, 34(7): 469–480.
Sun B., Ricardo-da-Silva J.M., and Spranger I. 1998. Critical factors of vanillin assay for catechins and proanthocyanidins. J. Agric. Food Chem. 46: 4267–4274.
Tootian Z., Louei Monfared A., Fazelipour S., Shybani M.T., Rouhollah F., Sasani F., and Molaemi E. 2012. Biochemical and structural changes of the kidney in mice exposed to phenol. Turk. J. Med. Sci. 42(4): 695–703.
Upasani C.D. and Balaraman R. 2003. Protective effect of Spirulina on lead induced deleterious changes in the lipid peroxidation and endogenous antioxidants in rats. Phytother. Res. 17(4): 330–334.
Vij A.G. 2009. Hemopoietic, hemostatic and mutagenic effects of lead and possible prevention by zinc and vitamin C. Al Ameen. J. Med. Sci. 2(2): 27–36.
Wang J., Yang Z., Lin L., Zhao Z., Liu Z., and Liu X. 2012. Protective effect of naringenin against lead-induced oxidative stress in rats. Biol. Trace Elem. Res. 146(3): 354–359.
Witko V., Nguyen A.T., and Descamps-Latscha B. 1992. Microtiter plate assay for phagocyte-derived taurine chloramines. J. Clin. Lab. Anal. 6(1): 47–53.
Yagi K. 1976. A simple fluorometric assay for lipoperoxide in blood plasma. Biochem. Med. 15(2): 212–216.
Yuliana N.D., Khatib A., Link-Struensee A.M., Ijzerman A.P., Rungkat-Zakaria F., Choi Y.H., and Verpoorte R. 2009. Adenosine A1 receptor binding activity of methoxy flavonoids from Orthosiphon stamineus. Planta Med. 75(2): 132–136.
Zhang Z., Gao X., Guo M., Jiang H., Cao Y., and Zhang N. 2017. The Protective effect of baicalin against lead-induced renal oxidative damage in mice. Biol. Trace Elem. Res. 175(1): 129–135.
Zou W., Yan M., Xu W., Huo H., Sun L., Zheng Z., and Liu X. 2001. Cobalt chloride induces PC12 cells apoptosis through reactive oxygen species and accompanied by AP-1 activation. J. Neurosci. Res. 64(6): 646–653.

Information & Authors


Published In

cover image Applied Physiology, Nutrition, and Metabolism
Applied Physiology, Nutrition, and Metabolism
Volume 44Number 3March 2019
Pages: 271 - 281


Received: 20 June 2018
Accepted: 7 August 2018
Accepted manuscript online: 23 August 2018
Version of record online: 23 August 2018


Request permissions for this article.

Key Words

  1. diet
  2. injury
  3. physiology
  4. stress
  5. therapy


  1. régime alimentaire
  2. dommages
  3. physiologie
  4. stress
  5. thérapie



Manel Gargouri* [email protected]
Laboratory of Animal Ecophysiology, Faculty of Sciences, University of Sfax, 3038 Sfax, Tunisia.
EA 7462 Géoarchitecture, Faculty of Sciences, University of Western Brittany, 6 Avenue V. Le Gorgeu, CS 93837, 29238 Brest Cedex 3, France.
Ahlem Soussi*
Laboratory of Animal Ecophysiology, Faculty of Sciences, University of Sfax, 3038 Sfax, Tunisia.
Amel Akrouti
Laboratory of Animal Ecophysiology, Faculty of Sciences, University of Sfax, 3038 Sfax, Tunisia.
Christian Magné
EA 7462 Géoarchitecture, Faculty of Sciences, University of Western Brittany, 6 Avenue V. Le Gorgeu, CS 93837, 29238 Brest Cedex 3, France.
Abdelfattah El Feki
Laboratory of Animal Ecophysiology, Faculty of Sciences, University of Sfax, 3038 Sfax, Tunisia.


These authors contributed equally to this work.
Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink.

Metrics & Citations


Other Metrics


Cite As

Export Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

1. Antioxidant compounds from the Arthrospira platensis protect against Bisphenol A-induced nephrotoxicity in rats
2. Effect of Spirulina platensis Supplementation on Reproductive Parameters of Sahrawi and Jabbali Goat Bucks
3. The effects of spirulina supplementation on serum iron and ferritin, anemia parameters, and fecal occult blood in adults with ulcerative colitis: A randomized, double-blinded, placebo-controlled trial
4. Spirulina (Arthrospira maxima) mitigates the toxicity induced by a mixture of metal and NSAID in Xenopus laevis
5. Effects of Dietary Supplementation of Spirulina platensis on the Immune System, Intestinal Bacterial Microbiome and Skin Traits of Mink
6. The Allium triquetrum L. Leaves Mitigated Hepatotoxicity and Nephrotoxicity Induced by Lead Acetate in Wistar Rats
7. Effects of Dietary Inclusion of Spirulina platensis on the Reproductive Performance of Female Mink
8. Protective role of flaxseed lignan secoisolariciresinol diglucoside against lead-acetate-induced oxidative-stress-mediated nephrotoxicity in rats
9. Lead in Synergism With IFNγ Acts on Bone Marrow-Resident Macrophages to Increase the Quiescence of Hematopoietic Stem Cells
10. Protein Carbonylation and Lipid Peroxidation in Hematological Malignancies
11. Protective effects of spirulina against hemato-biochemical alterations, nephrotoxicity, and DNA damage upon lead exposition
12. Coenzyme Q10 Activates the Antioxidant Machinery and Inhibits the Inflammatory and Apoptotic Cascades Against Lead Acetate-Induced Renal Injury in Rats
13. Therapeutic influences of almond oil on male rats exposed to a sublethal concentration of lead

View Options

Get Access

Login options

Check if you access through your login credentials or your institution to get full access on this article.


Click on the button below to subscribe to Applied Physiology, Nutrition, and Metabolism

Purchase options

Purchase this article to get full access to it.

Restore your content access

Enter your email address to restore your content access:

Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.

View options


View PDF

Full Text

View Full Text





Share Options


Share the article link

Share on social media