Investigation on the role of Spirulina platensis in ameliorating behavioural changes, thyroid dysfunction and oxidative stress in offspring of pregnant rats exposed to fluoride
Abstract
The study investigated the role of Spirulina platensis in reversing sodium fluoride-induced thyroid, neurodevelopment and oxidative alterations in offspring of pregnant rats. The total antioxidant activity, phycocyanins, and β carotene content were quantified in Spirulina. Thirty female pregnant rats were allocated to six groups and treatment initiated orally from embryonic day (ED) 6 to postnatal day (PND) 15. Treatment groups included control, Spirulina alone, sodium fluoride (20 mg/kg) alone, and sodium fluoride along with Spirulina (250 and 500 mg/kg). Serum fluoride levels were determined on ED 20 and PND 11. Offspring were subjected to behavioural testing, estimation of thyroid levels, oxidative measurements in brain mitochondrial fraction and histological evaluation of the cerebellum. Fluoride-induced alterations in thyroid hormones, behaviour and increased oxidative stress. Spirulina augmented the displacement of fluoride, facilitated antioxidant formation, improved behaviour and protected Purkinje cells. Supplementing Spirulina during pregnancy could reduce the risk of fluoride toxicity in offspring.
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Spirulina has high nutritional value due to its content in proteins, essential amino acids, minerals, essential fatty acids, vitamins, and liposoluble antioxidants.
“Spirulina has high nutritional values due to its content in proteins, essential amino acids, minerals, essential fatty acids, vitamins, and liposoluble antioxidants (vitamin E and carotenoids) [28–38]”
From Antioxidant, Immunomodulating, and Microbial‐Modulating Activities of the Sustainable and Ecofriendly <i>Spirulina</i> (2017) · cites this paper as [34]
Antioxidant activity accounts for the protective role of Spirulina against toxicity induced by carbon tetrachloride, metals, deltamethrin, and drugs in animal models.
“It has been suggested that the antioxidant activity accounts for the protective role of Spirulina against the toxicity induced by carbon tetrachloride (CCl4) [40], by metals (arsenic, mercuric chloride, chromium, cadmium, and fluoride) [34, 41–44], by the insecticide deltamethrin in mice [39] and rats [45]”
From Antioxidant, Immunomodulating, and Microbial‐Modulating Activities of the Sustainable and Ecofriendly <i>Spirulina</i> (2017) · cites this paper as [34]
Cites
PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 315,771 · see citing works
Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction
Ohkawa, H., Ohishi, N., & Yagi, K. (1979) · Analytical Biochemistry · doi:10.1016/0003-2697(79)90738-3 · Cited by 29,460 · see citing works
Aebi, H. (1984) · Methods in Enzymology · doi:10.1016/s0076-6879(84)05016-3 · Cited by 25,696 · see citing works
Misra, H. P., & Fridovich, I. (1972) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)45228-9 · Cited by 9,097 · see citing works
Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents
Lichtenthaler, H. K., & Wellburn, A. R. (1983) · Biochemical Society Transactions · doi:10.1042/bst0110591 · Cited by 6,813 · see citing works
Study and interpretation of the chemical characteristics of natural water
Hem, J. D. (1959) · doi:10.3133/wsp1473_ed1 · Cited by 5,769 · see citing works
[12] Assays of glutathione peroxidase
Flohé, L., & Günzler, W. A. (1984) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(84)05015-1 · Cited by 4,954 · see citing works
MORON, M., DePierre, J. W., & Mannervik, B. (1979) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(79)90289-7 · Cited by 4,214 · see citing works
Vegetables, Fruit, and Cancer Prevention
STEINMETZ, K. A., & POTTER, J. D. (1996) · Journal of the American Dietetic Association · doi:10.1016/s0002-8223(96)00273-8 · Cited by 2,118 · see citing works
Antioxidant activity of Nigella sativa essential oil
Burits, M., & Bučar, F. (2000) · Phytotherapy Research · doi:10.1002/1099-1573(200008)14:5 · Cited by 1,856 · see citing works
COMPLEMENTARY CHROMATIC ADAPTATION IN A FILAMENTOUS BLUE-GREEN ALGA
Bennett, A., & Bogorad, L. (1973) · The Journal of Cell Biology · doi:10.1083/jcb.58.2.419 · Cited by 1,773 · see citing works
Amarowicz, R., Pegg, R. B., Rahimi‐Moghaddam, P., Barl, B., & Weil, J. A. (2003) · Food Chemistry · doi:10.1016/s0308-8146(03)00278-4 · Cited by 1,179 · see citing works
Total antioxidant capacity as a tool to assess redox status: critical view and experimental data
Ghiselli, A., Serafini, M., Natella, F., & Scaccini, C. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(00)00394-4 · Cited by 1,102 · see citing works
Behavioral Alterations in Rats Prenatally Exposed to Valproic Acid: Animal Model of Autism
Schneider, T., & Przewłocki, R. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300518 · Cited by 959 · see citing works
Vegetable, Fruit, and Cereal Fiber Intake and Risk of Coronary Heart Disease Among Men
Rimm, E. B. (1996) · JAMA · doi:10.1001/jama.1996.03530300031036 · Cited by 889 · see citing works
The role of thyroid hormones in prenatal and neonatal neurological development--current perspectives
Porterfield, S. P. (1993) · Endocrine Reviews · doi:10.1210/er.14.1.94 · Cited by 679 · see citing works
The quantitative measurement of motor inco-ordination in naive mice using an accelerating rotarod
Jones, B. J., & Roberts, D. J. (1968) · Journal of Pharmacy and Pharmacology · doi:10.1111/j.2042-7158.1968.tb09743.x · Cited by 583 · see citing works
Dapkevicius, A., Venskutonis, R., van Beek, T. A., & Linssen, J. P. H. (1998) · Journal of the Science of Food and Agriculture · doi:10.1002/(sici)1097-0010(199805)77:1 · Cited by 573 · see citing works
Molecular Basis of Thyroid Hormone-Dependent Brain Development
Oppenheimer, J. H., & Schwartz, H. L. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.4.0309 · Cited by 517 · see citing works
Thyroid Hormones and Brain Development
Dussault, J. H., & Ruel, J. (1987) · Annual Review of Physiology · doi:10.1146/annurev.ph.49.030187.001541 · Cited by 500 · see citing works
Ausó, E., Lavado-Autric, R., Cuevas‐Romero, E., del Rey, F. E., de Escobar, G. M., & Berbel, P. J. (2004) · Endocrinology · doi:10.1210/en.2004-0274 · Cited by 454 · see citing works
Lead biosorption and desorption by intact and pretreated spirulina maxima biomass
Gong, R., Ding, Y., Liu, H., Chen, Q., & Liu, Z. (2004) · Chemosphere · doi:10.1016/j.chemosphere.2004.08.055 · Cited by 355 · see citing works
A Conceptual Overview on Sustainable Technologies for the Defluoridation of Drinking Water
Ayoob, S., Gupta, A., & Bhat, V. T. (2008) · Critical Reviews in Environmental Science and Technology · doi:10.1080/10643380701413310 · Cited by 335 · see citing works
Thyroid Hormone Action and Brain Development
Koibuchi, N., & Chin, W. W. (2000) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(00)00238-1 · Cited by 332 · see citing works
Neurotoxicity of sodium fluoride in rats
Mullenix, P. J., DenBesten, P. K., Schunior, A., & Kernan, W. J. (1995) · Neurotoxicology and Teratology · doi:10.1016/0892-0362(94)00070-t · Cited by 316 · see citing works
Antioxidant-rich diets improve cerebellar physiology and motor learning in aged rats
Bickford, P. C., Gould, T., Briederick, L., Chadman, K., Pollock, A., Young, D., Shukitt-Hale, B., & Joseph, J. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02280-0 · Cited by 298 · see citing works
Bhat, V. B., & Madyastha, K. M. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5195 · Cited by 277 · see citing works
Molecular Basis of Thyroid Hormone-Dependent Brain Development
Oppenheimer, J. H. (1997) · Endocrine Reviews · doi:10.1210/er.18.4.462 · Cited by 274 · see citing works
Thyroid Hormone Action in Neural Development
Thompson, C. C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.10.939 · Cited by 265 · see citing works
Fluoride contamination in groundwater in parts of Nalgonda District, Andhra Pradesh, India
Brindha, K., Rajesh, R., Ramasamy, M., et al. (2010) · Environmental Monitoring and Assessment · doi:10.1007/s10661-010-1348-0 · Cited by 254 · see citing works
Nabavi, S. M., Nabavi, S. F., Eslami, S., & Moghaddam, A. H. (2011) · Food Chemistry · doi:10.1016/j.foodchem.2011.11.070 · Cited by 244 · see citing works
Ferruzzi, M. G., Böhm, V., Courtney, P. D., & Schwartz, S. J. (2002) · Journal of Food Science · doi:10.1111/j.1365-2621.2002.tb08782.x · Cited by 238 · see citing works
Dietary supplementation with blueberries, spinach, or spirulina reduces ischemic brain damage
Wang, Y., Chang, C.-F., Chou, J., Chen, H.-L., Deng, X., Harvey, B. K., Cadet, J. L., & Bickford, P. C. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2004.12.014 · Cited by 223 · see citing works
Riss, J., Décordé, K., Sutra, T., Delage, M., Baccou, J.-C., Jouy, N., Brune, J.-P., Oréal, H., Cristol, J.-P., & Rouanet, J.-M. (2007) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf070529g · Cited by 208 · see citing works
Bhat, V. B., & Madyastha, K. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5368 · Cited by 206 · see citing works
Bermejo‐Bescós, P., Piñero, E., & Villar, Á. (2008) · Food Chemistry · doi:10.1016/j.foodchem.2008.02.021 · Cited by 204 · see citing works
Cheh, M. A., Millonig, J. H., Roselli, L. M., Ming, X., Jacobsen, E. P., Kamdar, S., & Wagner, G. C. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.086 · Cited by 190 · see citing works
Upasani, C. D., & Balaraman, R. (2003) · Phytotherapy Research · doi:10.1002/ptr.1135 · Cited by 158 · see citing works
Miller, S., Romano, C., & Cotman, C. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-09-06103.1995 · Cited by 135 · see citing works
Hassan, H. A., & Yousef, M. I. (2009) · Food and Chemical Toxicology · doi:10.1016/j.fct.2009.06.023 · Cited by 131 · see citing works
Influence of Chronic Fluorosis on Membrane Lipids in Rat Brain
Guan, Z., Wang, Y.-N., Xiao, K.-Q., Dai, D.-Y., Chen, Y., Liu, J., Sindelar, P. J., & Dallner, G. (1998) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(97)00136-0 · Cited by 131 · see citing works
Farwell, A. P., Dubord-Tomasetti, S. A., Pietrzykowski, A. Z., Stachelek, S. J., & Leonard, J. L. (2005) · Developmental Brain Research · doi:10.1016/j.devbrainres.2004.07.016 · Cited by 123 · see citing works
Oxidative stress in children with endemic skeletal fluorosis
Shivarajashankara, Y., Shivashankara, A., Rao, H. S., et al. (2001) · Cited by 119 · see citing works
Strömberg, I., Gemma, C., Vila, J., & Bickford, P. C. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.08.013 · Cited by 110 · see citing works
EXCESS FLUORIDE INGESTION AND THYROID HORMONE DERANGEMENTS IN CHILDREN LIVING IN DELHI, INDIA
Ak, S., & Bhatnagar, M. (2005) · Cited by 109 · see citing works
Nabavi, S. F., Nabavi, S. M., Habtemariam, S., Moghaddam, A. H., Sureda, A., Jafari, M., & Latifi, A. M. (2012) · Industrial Crops and Products · doi:10.1016/j.indcrop.2012.10.024 · Cited by 106 · see citing works
Reddy, G. B. (2003) · Toxicological Sciences · doi:10.1093/toxsci/kfg030 · Cited by 104 · see citing works
Ohl, F. (2003) · Clinical Neuroscience Research · doi:10.1016/s1566-2772(03)00084-7 · Cited by 97 · see citing works
Spirulina platensis feeding inhibited the anemia- and leucopenia-induced lead and cadmium in rats
Şimşek, N., Karadeniz, A., Kalkan, Y., Keleş, O. N., & Ünal, B. (2008) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2008.09.041 · Cited by 95 · see citing works
Effects of aging on cerebellar noradrenergic function and motor learning: nutritional interventions
Bickford, P. C., Shukitt‐Hale, B., & Joseph, J. A. (1999) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(99)00063-9 · Cited by 89 · see citing works
BRAIN LIPID PEROXIDATION AND ANTIOXIDANT SYSTEMS OF YOUNG RATS IN CHRONIC FLUORIDE INTOXICATION
Shivarajashankara, Y., Shivashankara, A., Bhat, G., et al. (2002) · Cited by 89 · see citing works
Thyroxine treatment and recovery of hypothyroidism-induced pyramidal cell damage
Ruiz‐Marcos, A., Sánchez-Toscano, F., Obregón, M.-J., del Rey, F. E., & de Escobar, G. M. (1982) · Brain Research · doi:10.1016/0006-8993(82)90530-3 · Cited by 81 · see citing works
Temporal stability of novelty exploration in mice exposed to different open field tests
Kalueff, A. V., Keisala, T., Minasyan, A., Kuuslahti, M., & Tuohimaa, P. (2006) · Behavioural Processes · doi:10.1016/j.beproc.2005.12.011 · Cited by 72 · see citing works
Fluoride induces apoptosis by caspase-3 activation in human leukemia HL-60 cells
Anuradha, C. D., Kanno, S., & Hirano, S. (2000) · Archives of Toxicology · doi:10.1007/s002040000132 · Cited by 69 · see citing works
Vincent, J., Legrand, C., Rabié, A., et al. (1984) · PubMed · Cited by 66 · see citing works
Spirulina as a source of vitamin A
Annapurna, V., Deosthale, Y. G., & Bamji, M. S. (1991) · Plant Foods for Human Nutrition · doi:10.1007/bf02194081 · Cited by 65 · see citing works
Effects of sodium fluoride on locomotor behavior and a few biochemical parameters in rats
Paul, V., Ekambaram, P., & Jayakumar, A. R. (1998) · Environmental Toxicology and Pharmacology · doi:10.1016/s1382-6689(98)00033-7 · Cited by 61 · see citing works
Oxidative stress induced by fluoride in adult mice and their suckling pups
Bouaziz, H., Croute, F., Boudawara, T. S., et al. (2007) · Experimental and Toxicologic Pathology · doi:10.1016/j.etp.2006.11.004 · Cited by 54 · see citing works
Paracetamol hepatotoxicity and microsomal function
Kaushal, R., Dave, K. R., & Katyare, S. S. (1999) · Environmental Toxicology and Pharmacology · doi:10.1016/s1382-6689(98)00053-2 · Cited by 39 · see citing works
FLUORIDE-INDUCED THYROID PROLIFERATIVE CHANGES AND THEIR REVERSAL IN FEMALE MICE AND THEIR PUPS
Bouaziz, H., Soussia, L., Guermazi, F., et al. (2005) · Cited by 39 · see citing works
Qin, G., Liu, Y., & Guan, Z. (2009) · Fluoride · Cited by 39 · see citing works
EFFECT OF FLUORIDE ON THYROID FUNCTION AND CEREBELLAR DEVELOPMENT IN MICE
Trabelsi, M., Guermazi, F., & Zeghal, N. (2001) · Cited by 38 · see citing works
Teas, J., Hébert, J. R., Fitton, J. H., & Zimba, P. V. (2004) · Medical Hypotheses · doi:10.1016/j.mehy.2003.10.005 · Cited by 38 · see citing works
Tri-iodothyronine regulates survival and differentiation of rat cerebellar granule neurons
Heisenberg, C., Thoenen, H., & Lindholm, D. (1992) · Neuroreport · doi:10.1097/00001756-199208000-00008 · Cited by 36 · see citing works
Potter, G. B., Facchinetti, F., Beaudoin, G. M. J., & Thompson, C. C. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-12-04373.2001 · Cited by 31 · see citing works
Kendall‐Taylor, P. (1972) · Journal of Endocrinology · doi:10.1677/joe.0.0540137 · Cited by 26 · see citing works
CHANGES IN ERYTHROCYTE PARAMETERS OF FLUOROTIC SHEEP
Yur, F., Belge, F., & Mert, N. (2003) · Van Yüzüncü Yıl University Academic Data Management System · Cited by 23 · see citing works
[Effects of chronic fluorosis on the thyroid gland].
Yu, Y. N. (1985) · PubMed · Cited by 14 · see citing works
Shao, Q., Wang, Y., & Guan, Z. (2000) · PubMed · Cited by 13 · see citing works
Effect of sodium fluoride on the thyroid gland of growing male albino rats
Selim, A. O., El-Haleem, M. R. A., & Ibrahim, I. H. (2012) · The Egyptian Journal of Histology · doi:10.1097/01.ehx.0000418503.12452.9a · Cited by 9 · see citing works
Goitre and fluorosis in Kenya.
Ao, O. (1982) · PubMed · Cited by 7 · see citing works
Carcoba, L. M., SANTIAGO, M., Moss, D. E., & Cabeza, R. D. J. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2007.09.008 · Cited by 2 · see citing works
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Wu, Q., Liu, L., Miron, A., Klímová, B., Wan, D., & Kuča, K. (2016) · Archives of Toxicology · doi:10.1007/s00204-016-1744-5 · Cited by 655 · see citing works
Finamore, A., Palmery, M., Bensehaila, S., & Peluso, I. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/3247528 · Cited by 256 · see citing works
‘Nutritional and healthical aspects of spirulina (Arthrospira) for poultry, animals and human.
Farag, M. R., Alagawany, M., Abd El-Hac, M. E., & Dhama, K. (2015) · International Journal of Pharmacology · doi:10.3923/ijp.2016.36.51 · Cited by 117 · see citing works
Elshazly, M. O., Abd El-Rahman, S. S., Morgan, A. M., & Ali, M. E. (2015) · PLOS ONE · doi:10.1371/journal.pone.0126780 · Cited by 31 · see citing works
- Authors
- Banji, D., Banji, O. J. F., Pratusha, N. G., & Annamalai, A. R.
- Affiliations
- Annamalai University (IN)
- Corresponding author
- Banji, David
- Venue
- Food Chemistry
- Publisher
- Elsevier BV
- Published
- 2013-09
- Volume
- 140
- Issue
- 1-2
- Pages
- 321-331
- ISSN
- 0308-8146 (ISSN-L)
- OpenAlex
- W1966852919
- Cited by
- 83
- References
- 72
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 6 · 2023: 10 · 2022: 10 · 2021: 6 · 2020: 5 · 2019: 8 · 2018: 7 · 2017: 5 · 2016: 4 · 2015: 7 · 2014: 2 · 2013: 2
- FWCI
- 3.87
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Food Chemistry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Universidad Nacional de Colombia
- Topics
- Physical Sciences › Environmental Science › Water Science and Technology › Fluoride Effects and Removal
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Heavy Metal Exposure and Toxicity
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Aluminum toxicity and tolerance in plants and animals
- Keywords
- Spirulina platensis, sodium fluoride, fluoride toxicity, prenatal exposure, offspring neurodevelopment, thyroid dysfunction, oxidative stress, behavior change, phycocyanin, beta-carotene, antioxidant activity, Purkinje cells, cerebellum, mitochondrial oxidative stress
- MeSH terms
- Animals, Antioxidants, Behavior, Brain, Female, Humans, Male, Phycocyanin, Pregnancy, Prenatal Exposure Delayed Effects, Sodium Fluoride, Thyroid Gland, Thyroid Hormones, Rats, Wistar, Oxidative Stress, Maternal Exposure, beta Carotene, Dietary Supplements, Rats, Spirulina
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