Maternal Spirulina supplementation during pregnancy and lactation partially prevents oxidative stress, glial activation and neuronal damage in protein malnourished F1 progeny
Abstract
Protein malnutrition (PMN) is a global health issue but most prevalent in Africa and Asia. It exerts detrimental effect on structural and physiological aspects of hippocampal circuitry. Despite accumulating evidence for PMN induced changes in nervous system, relatively very little is known about how maternal nutritional supplementation during malnutrition affects glial cells and neurons. Herein, we aimed to investigate the effects of maternal Spirulina supplementation against PMN induced oxidative stress, reactive gliosis and neuronal damage in hippocampus of F1 progeny. Three months old healthy Sprague Dawley females (n=24) were shifted to normoprotein (NC; 20% protein) and low protein (LP; 8% protein) diets 15 days before conception. The NC and LP group females were subdivided into two groups according to Spirulina supplementation (400 mg/kg/b.wt. orally throughout gestation and lactation period): normal control with Spirulina (NC SPI) and low protein with Spirulina supplemented group (LP SPI). F1 progeny born were used in present study. Thus, building on earlier results of ameliorated neurobehavioral and cognitive abilities in Spirulina supplemented protein deprived rats, the present study incorporates neurochemical and morphometric analysis of glial cells and neurons and revealed that maternal Spirulina consumption partially prevented the PMN associated neuropathological alterations in terms of attenuated oxidative brain damage, reduced reactive gliosis and apoptotic cell population, improved dendritic branch complexity with few damaged neurons and enhanced mushroom shaped spine density. The results suggest that cellular changes in hippocampus after PMN are partially restored after maternal Spirulina supplementation and one could envision intervention approaches using Spirulina against malnutrition.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Maternal dietary supplementation with Spirulina during pregnancy and lactation to protein-malnourished rats reduced astrocytic and microglial activation in F1 progeny.
“In another study, Sinha et al. observed that maternal dietary supplementation with Spirulina during pregnancy, and lactation to protein-malnourished (PMN) rats reduced astrocytic and microglial activation in F1 progeny.”
From Beneficial Effects of Spirulina Consumption on Brain Health (2022) · cites this paper as [64]
Spirulina caused a reduction of CR3 and MHC II expression on microglia cells.
“In addition, it was reported that Spirulina caused a reduction of CR3 and MHC II expression on microglia cells that lose the typical shape of activated phagocytic cells.”
From Beneficial Effects of Spirulina Consumption on Brain Health (2022) · cites this paper as [64]
Spirulina prevented PMN-induced astrogliosis by reducing the astrocytic population labeled with GFAP and S100β.
“In particular, Spirulina prevented PMN-induced astrogliosis by effectively reducing the astrocytic population labeled with glial fibrillary acidic protein (GFAP) and S100β, and with enlarged cell body and thick processes, a morphology that characterizes activated astrocytes.”
From Beneficial Effects of Spirulina Consumption on Brain Health (2022) · cites this paper as [64]
Spirulina treatment enhanced behavioral and cognitive functions in PMN rats.
“thus enhancing behavioral and cognitive functions [64].”
From Beneficial Effects of Spirulina Consumption on Brain Health (2022) · cites this paper as [64]
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
Aebi, H. (1984) · Methods in Enzymology · doi:10.1016/s0076-6879(84)05016-3 · Cited by 25,696 · see citing works
The 2007 WHO Classification of Tumours of the Central Nervous System
Louis, D. N., Ohgaki, H., Wiestler, O. D., Cavenee, W. K., Burger, P. C., Jouvet, A., Scheithauer, B. W., & Kleihues, P. (2007) · Acta Neuropathologica · doi:10.1007/s00401-007-0243-4 · Cited by 15,422 · 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
Neurotoxic reactive astrocytes are induced by activated microglia
Liddelow, S. A., Guttenplan, K. A., Clarke, L. E., Bennett, F. C., Bohlen, C. J., Schirmer, L., Bennett, M. L., Münch, A. E., Chung, W.-S., Peterson, T. C., et al. (2017) · Nature · doi:10.1038/nature21029 · Cited by 7,971 · see citing works
ROS function in redox signaling and oxidative stress
Schieber, M., & Chandel, N. S. (2014) · Current Biology · doi:10.1016/j.cub.2014.03.034 · Cited by 6,931 · see citing works
Oxidative stress, aging, and diseases
Liguori, I., Russo, G., Curcio, F., Bulli, G., Aran, L., Della-Morte, D., Gargiulo, G., Testa, G., Cacciatore, F., Bonaduce, D., et al. (2018) · Clinical Interventions in Aging · doi:10.2147/cia.s158513 · Cited by 3,979 · see citing works
Uttara, B., Singh, A., Zamboni, P., & Mahajan, R. (2009) · Current Neuropharmacology · doi:10.2174/157015909787602823 · Cited by 3,378 · see citing works
Dendritic organization in the neurons of the visual and motor cortices of the cat.
Sholl, D. A. (1953) · Europe PMC (PubMed Central) · Cited by 2,204 · see citing works
Microglial physiology: unique stimuli, specialized responses
Ransohoff, R. M., & Perry, V. H. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.021908.132528 · Cited by 1,858 · see citing works
Astrocytes, from brain glue to communication elements: the revolution continues
Volterra, A., & Meldolesi, J. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1722 · Cited by 1,763 · see citing works
JACOBSON, L., & SAPOLSKY, R. (1991) · Endocrine Reviews · doi:10.1210/edrv-12-2-118 · Cited by 1,739 · see citing works
Diversity of structures and properties among catalases
Chelikani, P., Fita, I., & Loewen, P. C. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-003-3206-5 · Cited by 1,701 · see citing works
Decreased Dendritic Spine Density on Prefrontal Cortical Pyramidal Neurons in Schizophrenia
Glantz, L. A., & Lewis, D. A. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.1.65 · Cited by 1,636 · see citing works
Reactive Oxygen Radicals in Signaling and Damage in the Ischemic Brain
Chan, P. H. (2001) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200101000-00002 · Cited by 1,589 · see citing works
Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease
Prinz, M., & Priller, J. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3722 · Cited by 1,329 · see citing works
Innate immunity in the central nervous system
Ransohoff, R. M., & Brown, M. A. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58644 · Cited by 1,034 · see citing works
Selective neuronal vulnerability to oxidative stress in the brain
Wang, X. (2010) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2010.00012 · Cited by 1,008 · see citing works
Emerging roles of astrocytes in neural circuit development
Clarke, L. E., & Barres, B. A. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3484 · Cited by 975 · see citing works
DeFelipe, J., & Fariñas, I. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90015-7 · Cited by 975 · see citing works
Early Life Programming and Neurodevelopmental Disorders
Bale, T. L., Baram, T. Z., Brown, A. S., Goldstein, J. M., Insel, T. R., McCarthy, M. M., Nemeroff, C. B., Reyes, T. M., Simerly, R. B., Susser, E. S., et al. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.028 · Cited by 961 · see citing works
Hol, E. M., & Pekny, M. (2015) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2015.02.004 · Cited by 917 · see citing works
The Emerging Role of Glutamate in the Pathophysiology and Treatment of Schizophrenia
GOFF, D. C., & Coyle, J. T. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.9.1367 · Cited by 914 · see citing works
Astrocytes Control Synapse Formation, Function, and Elimination
Chung, W.-S., Allen, N. J., & Eroglu, C. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020370 · Cited by 839 · see citing works
Interrelation of Oxidative Stress and Inflammation in Neurodegenerative Disease: Role of TNF
Fischer, R., & Maier, O. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/610813 · Cited by 744 · see citing works
The antioxidant, immunomodulatory, and anti-inflammatory activities of Spirulina: An overview
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
Fillman, S. G., Cloonan, N., Catts, V. S., Miller, L. C., Wong, J., McCrossin, T., Cairns, M., & Weickert, C. S. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.110 · Cited by 609 · see citing works
Dendritic spine pathology in schizophrenia
Glausier, J. R., & Lewis, D. A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.044 · Cited by 581 · see citing works
Superoxide dismutases—A review of the metal-associated mechanistic variations
Abreu, I. A., & Cabelli, D. E. (2010) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2009.11.005 · Cited by 563 · see citing works
Microglial cell dysregulation in brain aging and neurodegeneration
von Bernhardi, R., Eugenín-von Bernhardi, L., & Eugenín, J. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2015.00124 · Cited by 556 · see citing works
The role of the hippocampus in flexible cognition and social behavior
Rubin, R. D., Watson, P. D., Duff, M. C., & Cohen, N. J. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00742 · Cited by 489 · see citing works
Solleiro-Villavicencio, H., & Rivas-Arancibia, S. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00114 · Cited by 463 · see citing works
Antioxidant activity of different fractions of Spirulina platensis protean extract
Piñero Estrada, J. (2001) · Il Farmaco · doi:10.1016/s0014-827x(01)01084-9 · Cited by 447 · see citing works
Crosstalk Between Astrocytes and Microglia: An Overview
Matejuk, A., & Ransohoff, R. M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01416 · Cited by 445 · see citing works
Oxidative stress and human diseases: Origin, link, measurement, mechanisms, and biomarkers
Giustarini, D., Dalle‐Donne, I., Tsikas, D., & Rossi, R. (2009) · Critical Reviews in Clinical Laboratory Sciences · doi:10.3109/10408360903142326 · Cited by 443 · see citing works
Redox regulation of glial inflammatory response to lipopolysaccharide and interferonγ
Pawate, S., Shen, Q., Fan, F., & Bhat, N. R. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20180 · Cited by 428 · see citing works
Potential markers of oxidative stress in stroke
Cherubini, A., Ruggiero, C., Polidori, M. C., & Mecocci, P. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.06.025 · Cited by 427 · see citing works
Free radicals, antioxidant defense systems, and schizophrenia
Wu, J. Q., Kosten, T. R., & Zhang, X. Y. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.02.015 · Cited by 420 · see citing works
Ranjekar, P. K., Hinge, A. S., Hegde, M. V., Ghate, M. R., Kale, A. A., Sitasawad, S. L., Wagh, U. V., Debsikdar, V. B., & Mahadik, S. P. (2003) · Psychiatry Research · doi:10.1016/s0165-1781(03)00220-8 · Cited by 395 · see citing works
Effects of prenatal protein malnutrition on the hippocampal formation
Morgane, P. J., Mokler, D. J., & Galler, J. R. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00012-x · Cited by 391 · see citing works
Astrocyte phenotype in relation to Alzheimer‐type pathology in the ageing brain
Simpson, J. E., Ince, P. G., Lace, G., Forster, G., Shaw, P. J., Matthews, F., Savva, G., Brayne, C., & Wharton, S. B. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.05.015 · Cited by 381 · see citing works
Role of Redox Signaling in Neuroinflammation and Neurodegenerative Diseases
Hsieh, H., & Yang, C. (2013) · BioMed Research International · doi:10.1155/2013/484613 · Cited by 370 · see citing works
Postmortem evidence of cerebral inflammation in schizophrenia: a systematic review
Trépanier, M. O., Hopperton, K. E., Mizrahi, R., Mechawar, N., & Bazinet, R. P. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.90 · Cited by 360 · see citing works
Bisht, K., Sharma, K. P., & Tremblay, M. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.05.003 · Cited by 351 · see citing works
Spirulina in Clinical Practice: Evidence‐Based Human Applications
Karkos, P. D., Leong, S. C., Karkos, C. D., Sivaji, N., & Assimakopoulos, D. A. (2008) · Evidence-based Complementary and Alternative Medicine · doi:10.1093/ecam/nen058 · Cited by 332 · see citing works
Radical changes in multiple sclerosis pathogenesis
van Horssen, J., Witte, M. E., Schreibelt, G., & de Vries, H. E. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.06.011 · Cited by 322 · see citing works
Targeting Oxidative Stress in Central Nervous System Disorders
Patel, M. (2016) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2016.06.007 · Cited by 312 · see citing works
Prenatal Nutritional Deficiency and Risk of Adult Schizophrenia
Brown, A. S., & Susser, E. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn096 · Cited by 290 · see citing works
Evidence for a wide extra-astrocytic distribution of S100B in human brain
Steiner, J. H., Bernstein, H., Bielau, H., Berndt, A., Brisch, R., Mawrin, C., Keilhoff, G., & Bogerts, B. (2007) · BMC Neuroscience · doi:10.1186/1471-2202-8-2 · Cited by 282 · see citing works
Belay, A. (2002) · Medical Entomology and Zoology · Cited by 277 · see citing works
Monk, C. E., Georgieff, M., & Osterholm, E. A. (2012) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12000 · Cited by 260 · see citing works
Caspase-3 in the central nervous system: beyond apoptosis
D’Amelio, M., Sheng, M., & Cecconi, F. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.06.004 · Cited by 256 · see citing works
Human astrocytes in the diseased brain
Dossi, E., Vasile, F., & Rouach, N. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.02.001 · Cited by 250 · see citing works
Kamphuis, W., Middeldorp, J., Kooijman, L., Sluijs, J., Kooi, E., Moeton, M., Freriks, M., Mizee, M. R., & Hol, E. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.09.035 · Cited by 240 · see citing works
Herken, H., Uz, E., Özyurt, H., Söğüt, S., Vırıt, O., & Akyol, Ö. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000789 · Cited by 238 · see citing works
Prenatal Malnutrition and Adult Schizophrenia: Further Evidence From the 1959-1961 Chinese Famine
Xu, M.-Q., Sun, W.-S., Liu, B.-X., Feng, G.-Y., Yu, L., Yang, L. H., He, G., Sham, P. C., Susser, E., Clair, D. S., et al. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn168 · Cited by 238 · see citing works
Microglial activation and progressive brain changes in schizophrenia
Laskaris, L., Biase, M. A. D., Everall, I., Chana, G., Christopoulos, A., Skafidas, E. S., Cropley, V., & Pantelis, C. (2015) · British Journal of Pharmacology · doi:10.1111/bph.13364 · Cited by 227 · see citing works
Caspase-3 activation as a bifurcation point between plasticity and cell death
Snigdha, S., Smith, E. D., Prieto, G. A., & Cotman, C. W. (2012) · Neuroscience Bulletin · doi:10.1007/s12264-012-1057-5 · Cited by 227 · see citing works
Grosshagauer, S., Kraemer, K., & Somoza, V. (2020) · Journal of agricultural and food chemistry · doi:10.1021/acs.jafc.9b08251 · Cited by 216 · see citing works
NUTRITIONAL AND TOXICOLOGICAL ASPECTS OF SPIRULINA (ARTHROSPIRA).
Gutiérrez-Salmeán, G., Castillo, L., & Chamorro, G. (2015) · PubMed · doi:10.3305/nh.2015.32.1.9001 · Cited by 212 · see citing works
Jarskog, L. F., Selinger, E. S., Lieberman, J. A., & Gilmore, J. H. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.1.109 · Cited by 205 · see citing works
Evaluation of Microalgae for use as Nutraceuticals and Nutritional Supplements
Bishop, W. M., & Zubeck, H. M. (2012) · Journal of Nutrition & Food Sciences · doi:10.4172/2155-9600.1000147 · Cited by 203 · see citing works
Kim, Y. H., Park, J., & Choi, Y. K. (2019) · Antioxidants · doi:10.3390/antiox8050121 · Cited by 203 · see citing works
Dendritic Spine Pathology in Neurodegenerative Diseases
Herms, J., & Dorostkar, M. M. (2016) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-012615-044216 · Cited by 201 · see citing works
Dendritic spine alterations in schizophrenia
Moyer, C. E., Shelton, M. A., & Sweet, R. A. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.11.042 · Cited by 184 · see citing works
United States Pharmacopeia Safety Evaluation of Spirulina
Marles, R. J., Barrett, M. L., Barnes, J., Chavez, M. L., Gardiner, P., Ko, R., Mahady, G. B., Dog, T. L., Sarma, N. D., Giancaspro, G. I., et al. (2011) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408391003721719 · Cited by 177 · see citing works
Advances in methods for the determination of biologically relevant lipid peroxidation products
Spickett, C. M., Wiswedel, I., Siems, W., Žarković, K., & Žarković, N. (2010) · Free Radical Research · doi:10.3109/10715762.2010.498476 · Cited by 152 · see citing works
Increased expression of astrocyte markers in schizophrenia: Association with neuroinflammation
Catts, V. S., Wong, J., Fillman, S. G., Fung, S. J., & Weickert, C. S. (2014) · Australian & New Zealand Journal of Psychiatry · doi:10.1177/0004867414531078 · Cited by 148 · see citing works
Dendritic Spines as Tunable Regulators of Synaptic Signals
Tønnesen, J., & Nägerl, U. V. (2016) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2016.00101 · Cited by 136 · see citing works
Fahrner, A., Kann, G., Flubacher, A., Heinrich, C., Freiman, T. M., Zentner, J., Frotscher, M., & Haas, C. A. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.08.023 · Cited by 133 · see citing works
Nutrition rehabilitation of undernourished children utilizing Spiruline and Misola
Simpore, J., Kabore, F., Zongo, F., Dansou, D., Bere, A., Pignatelli, S., Biondi, D. M., Ruberto, G., & Musumeci, S. (2006) · Nutrition Journal · doi:10.1186/1475-2891-5-3 · Cited by 125 · see citing works
Dendritic spines do not split during hippocampal LTP or maturation
Fiala, J. C., Allwardt, B. A., & Harris, K. M. (2002) · Nature Neuroscience · doi:10.1038/nn830 · Cited by 124 · see citing works
Wierzba‐Bobrowicz, T., Lewandowska, E., Lechowicz, W., Stępień, T., & Pasennik, E. (2005) · PubMed · Cited by 113 · see citing works
Selective immunolesions of hippocampal cholinergic input fail to impair spatial working memory
McMahan, R. W., Sobel, T. J., & Baxter, M. G. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:2 · Cited by 109 · see citing works
Fractionation of lipids and purification of γ-linolenic acid (GLA) from Spirulina platensis
Sajilata, M. G., Singhal, R. S., & Kamat, M. Y. (2008) · Food Chemistry · doi:10.1016/j.foodchem.2008.01.005 · Cited by 105 · see citing works
Garbarino, V. R., Orr, M. E., Rodriguez, K. A., & Buffenstein, R. (2015) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2015.01.029 · Cited by 104 · see citing works
Maternal protein restriction early in rat pregnancy alters brain development in the progeny
Gressèns, P., Muaku, S. M., Besse, L., Nsegbe, É., Gallego, J., Delpech, B., Gaultier, C., Evrard, P., Ketelslegers, J., & Maiter, D. M. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)00109-0 · Cited by 94 · see citing works
Dendritic Spine Pathology in Infants With Severe Protein-Calorie Malnutrition
Benı́tez-Bribiesca, L., la Rosa-Alvarez, I. D., & Mansilla‐Olivares, A. (1999) · PEDIATRICS · doi:10.1542/peds.104.2.e21 · Cited by 93 · see citing works
Interplay of Amygdala and Cingulate Plasticity in Emotional Fear
Toyoda, H., Li, X., Wu, L., Zhao, M., Descalzi, G., Chen, T., Koga, K., & Zhuo, M. (2011) · Neural Plasticity · doi:10.1155/2011/813749 · Cited by 85 · see citing works
Antioxidant and Anticancer Activity of Spirulina platensis Water Extracts
Zaid, A. A. A., Hammad, D. M., & Sharaf, E. M. (2015) · International Journal of Pharmacology · doi:10.3923/ijp.2015.846.851 · Cited by 81 · see citing works
Antioxidant status in children with protein-energy malnutrition (PEM) living in Cairo, Egypt
Ashour, M. N., Salem, S. I., El-Gadban, H., Elwan, N., & Basu, T. K. (1999) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1600830 · Cited by 77 · see citing works
The novel oxidative stress marker thioredoxin is increased in first-episode schizophrenic patients
Zhang, X., Chen, D. C., Xiu, M. H., Wang, F., Qi, L. Y., Sun, H. Q., Chen, S., He, S. C., Wu, G. Y., Haile, C. N., et al. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.05.016 · Cited by 76 · see citing works
de Oliveira, J. C., Lisboa, P. C., de Moura, E. G., Barella, L. F., Miranda, R. A., Malta, A., Franco, C. C. D. S., Ribeiro, T. A., Torrezan, R., Gravena, C., et al. (2012) · Journal of Endocrinology · doi:10.1530/joe-12-0408 · Cited by 73 · see citing works
Systematic Review and Meta-Analysis of Circulating S100B Blood Levels in Schizophrenia
Aleksovska, K., Leoncini, E., Bonassi, S., Cesario, A., Boccia, S., & Frustaci, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106342 · Cited by 72 · see citing works
Bachstetter, A. D., Jernberg, J., Schlunk, A., Vila, J. L., Hudson, C., Cole, M. J., Shytle, R. D., Tan, J., Sanberg, P. R., Sanberg, C. D., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010496 · Cited by 71 · see citing works
Effects of protein deprivation on pyramidal cells of the visual cortex in rats of three age groups
Díaz-Cintra, S. Y., Cintra, L., Ortega, A., Kemper, T. L., & Morgane, P. J. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902920108 · Cited by 69 · see citing works
Al-chalabi, B. M., Thanoon, I. A. J., & Ahmed, F. A. (2009) · Neuropsychobiology · doi:10.1159/000202823 · Cited by 66 · see citing works
Self-organization of multiple spatial and context memories in the hippocampus
Stella, F., Cerasti, E., Si, B., Ježek, K., & Treves, A. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.12.002 · Cited by 63 · see citing works
Effect of protein malnutrition on CA3 hippocampal pyramidal cells in rats of three ages
García-Ruiz, M., Díaz-Cintra, S. Y., Cintra, L., & Corkidi, G. (1993) · Brain Research · doi:10.1016/0006-8993(93)91060-6 · Cited by 59 · see citing works
Khalil, S. R., Khalifa, H. A., Abdel-Motal, S. M., Mohammed, H., Elewa, Y. H. A., & Mahmoud, H. A. (2018) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2018.03.068 · Cited by 52 · see citing works
Free Radicals and Antioxidant Status in Protein Energy Malnutrition
Khare, M., Mohanty, C., Das, B. K., Jyoti, A., Mukhopadhyay, B., & Mishra, S. P. (2014) · International Journal of Pediatrics · doi:10.1155/2014/254396 · Cited by 49 · see citing works
Sinha, S., Patro, N., & Patro, I. K. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00966 · Cited by 49 · see citing works
Self-citationAzabji-Kenfack, M., Dikosso, S. E., Loni, E. G., Onana, E. A., Sobngwi, E., Gbaguidi, E., Kana, A. L. N., Nguefack-Tsague, G., Von der Weid, D., Njoya, O., et al. (2011) · Nutrition and Metabolic Insights · doi:10.4137/nmi.s5862 · Cited by 48 · see citing works
Feóli, A. M. P., Siqueira, I. R., de Almeida, L. M. V., Tramontina, A. C., Battú, C. E., Wofchuk, S. T., Gottfried, C., Perry, M. L. S., & Gonçalves, C. (2006) · Journal of Nutrition · doi:10.1093/jn/136.9.2357 · Cited by 47 · see citing works
Some effects of protein‐calorie undernutrition on the developing central nervous system of the rat
Noback, C. R., & Eisenman, L. M. (1981) · The Anatomical Record · doi:10.1002/ar.1092010109 · Cited by 45 · see citing works
Andrade, J. P., Castanheira-Vale, A. J., Paz-Dias, P. G., Madeira, M. D., & Paula-Barbosa, M. M. (1996) · Experimental Brain Research · doi:10.1007/bf00229626 · Cited by 44 · see citing works
Protein Malnutrition and Brain Development
Chertoff, M. (2015) · Brain Disorders & Therapy · doi:10.4172/2168-975x.1000171 · Cited by 43 · see citing works
Jacobsson, S. O. P., Cassel, G. E., & Persson, S.-&. (1999) · Archives of Toxicology · doi:10.1007/s002040050616 · Cited by 42 · see citing works
Sinha, S., Patro, N., & Patro, I. K. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.08.181 · Cited by 39 · see citing works
Self-citationOxidative stress status in nutritionally stunted children
Aly, G. S., Shaalan, A., Mattar, M. K., Ahmed, H. H., Zaki, M. E., & Abdallah, H. R. (2014) · Egyptian Pediatric Association Gazette · doi:10.1016/j.epag.2014.02.003 · Cited by 37 · see citing works
Reyes‐Castro, L. A., Padilla‐Gómez, E., Parga‐Martínez, N. J., Castro‐Rodríguez, D. C., Quirarte, G. L., Díaz‐Cintra, S., Nathanielsz, P. W., & Zambrano, E. (2018) · Hippocampus · doi:10.1002/hipo.22798 · Cited by 36 · see citing works
Moradikor, N., Ghanbari, A., Rashidipour, H., Yousefi, B., Bandegi, A. R., & Rashidy‐Pour, A. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.03.004 · Cited by 36 · see citing works
A Sequential Study of Age-Related Lipofuscin Accumulation in Hippocampus and Striate Cortex of Rats
Singh Kushwaha, S., Patro, N., & Kumar Patro, I. (2018) · Annals of Neurosciences · doi:10.1159/000490908 · Cited by 35 · see citing works
Self-citationHernández, A., Burgos, H., Mondaca, M., Barra, R., Núñez, H., Pérez, H., Soto‐Moyano, R., Sierralta, W. D., Fernández, V., Olivares, R., et al. (2008) · Neural Plasticity · doi:10.1155/2008/646919 · Cited by 33 · see citing works
Matondo, F. K., Takaisi, K., Nkuadiolandu, A. B., Kazadi Lukusa, A., & Aloni, M. N. (2016) · International Journal of Pediatrics · doi:10.1155/2016/1296414 · Cited by 33 · see citing works
Masuda, K., & Chitundu, M. (2019) · PLoS ONE · doi:10.1371/journal.pone.0211693 · Cited by 33 · see citing works
Supplementary effect of spirulina on hematological status of rats during pregnancy and lactation
Kapoor, R., & Mehta, U. (1998) · Plant Foods for Human Nutrition · doi:10.1023/a:1008027408919 · Cited by 32 · see citing works
Patro, N., Naik, A. A., & Patro, I. K. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1065-1 · Cited by 30 · see citing works
Self-citationEvaluation of the toxicity of Arthrospira (Spirulina) platensis extract
Hutadilok-Towatana, N., Reanmongkol, W., & Panichayupakaranant, P. (2010) · Journal of Applied Phycology · doi:10.1007/s10811-009-9499-5 · Cited by 24 · see citing works
Intra-generational protein malnutrition impairs temporal astrogenesis in rat brain
Naik, A. A., Patro, N., Seth, P., & Patro, I. K. (2017) · Biology Open · doi:10.1242/bio.023432 · Cited by 21 · see citing works
Self-citationQuick Golgi method: modified for high clarity and better neuronal anatomy.
Patro, N., Kumar, K., & Patro, I. K. (2013) · PubMed · Cited by 15 · see citing works
Self-citationSpirulina Effectiveness Study on Child Malnutrition in Zambia
Masuda, K., Inoue, Y., Inoue, R., Nakamura, A., Chitundu, M., Murakami, J., Ota, Y., & Matsugami, J. (2014) · OpenDocs (Institute of Development Studies) · Cited by 15 · see citing works
[Protective effects of spirulina on hippocampal injury in exercise-fatigue mice and its mechanism].
Zhu, H.-Z., Zhang, Y., Mei-ju, Z., Wu, R., & Zeng, Z.-G. (2018) · PubMed · doi:10.12047/j.cjap.5695.2018.126 · Cited by 6 · see citing works
Increased Lymphocyte Caspase-3 Activity in Patients with Schizophrenia
Lazarevic, D. S., Đorđević, V. V., Ćosić, V., Vlahović, P., Tošić-Golubović, S., Ristić, T., & Đorđević, V. B. (2010) · Journal of Medical Biochemistry · doi:10.2478/v10011-011-0002-x · Cited by 5 · see citing works
Possible role of oxidative stress in malnourished children.
Perampalli, T., Swami, S. C., Kumbar, K. M., Suryakar, A. N., & Shaikh, A. K. (2010) · Current Pediatric Research · Cited by 5 · see citing works
Sharma, S., & Mishra, A. K. (2017) · International Journal of Pharma and Bio Sciences · doi:10.22376/ijpbs.2017.8.4.b461-470 · Cited by 5 · see citing works
Lattke, M., & Wirth, T. (2018) · InTech eBooks · doi:10.5772/intechopen.72283 · Cited by 4 · see citing works
Rosoklija, G., Toomayan, G., Ellis, S. P., Keilp, J., Mann, J. J., Latov, N., Hays, A. P., & Dwork, A. J. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.4.349 · Cited by 1 · see citing works
Flagged first, then by citations
1 of the 119 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Functional Properties of Bioactive Compounds from Spirulina spp.: Current Status and Future Trends
Bortolini, D. G., Maciel, G. M., Fernandes, I. D. A. A., Pedro, A. C., Rubio, F. T. V., Branco, I. G., & Haminiuk, C. W. I. (2022) · Food Chemistry: Molecular Sciences · doi:10.1016/j.fochms.2022.100134 · Cited by 201 · see citing works
Beneficial Effects of Spirulina Consumption on Brain Health
Trotta, T., Porro, C., Cianciulli, A., & Panaro, M. A. (2022) · Nutrients · doi:10.3390/nu14030676 · Cited by 98 · see citing works
Wide range applications of spirulina: from earth to space missions
Fais, G., Manca, A., Bolognesi, F., Borselli, M., Concas, A., Busutti, M., Broggi, G., Sanna, P., Castillo-Aleman, Y. M., Rivero-Jiménez, R. A., et al. (2022) · Marine Drugs · doi:10.3390/md20050299 · Cited by 98 · see citing works
Spirulina Microalgae and Brain Health: A Scoping Review of Experimental and Clinical Evidence
Sorrenti, V., Castagna, D. A., Fortinguerra, S., Buriani, A., Scapagnini, G., & Willcox, D. C. (2021) · Marine Drugs · doi:10.3390/md19060293 · Cited by 94 · see citing works
Gogna, S., Kaur, J., Sharma, K., Prasad, R., Singh, J., Bhadariya, V., Kumar, P., & Jarial, S. (2023) · Journal of the American Nutrition Association · doi:10.1080/27697061.2022.2103852 · Cited by 83 · see citing works
Spirulina, an FDA-approved functional food: Worth the hype?
Ahmad, A. M. R., Intikhab, A., Zafar, S., Farooq, U., Shah, S. H. B. U., Akram, S., Abid, J., Parveen, Z., & Iqbal, S. (2023) · Cellular and Molecular Biology · doi:10.14715/cmb/2022.69.1.24 · Cited by 32 · see citing works
Phycochemistry and pharmacological significance of filamentous cyanobacterium Spirulina sp.
Sabat, S., Bej, S., Swain, S. N., Bishoyi, A. K., Sahoo, C. R., Sabat, G., & Padhy, R. N. (2025) · Bioresources and Bioprocessing · doi:10.1186/s40643-025-00861-0 · Cited by 31 · see citing works
Neuro-nutraceuticals: Natural products nourish the brain but be aware of contrary effects
Williams, R. J., Mohanakumar, K. P., & Beart, P. M. (2021) · Neurochemistry International · doi:10.1016/j.neuint.2021.105159 · Cited by 12 · see citing works
Beneficial Effects of Spirulina on Brain Health: A Systematic Review
Kumar, S., Saha, S., Singh, K., Singh, T., Miahra, A. K., Dubey, B. N., & Singh, S. (2024) · Current Functional Foods · doi:10.2174/0126668629269256231222092721 · Cited by 11 · see citing works
Tavares, J., Oliveira, A. V., Nascimento, T. D. S., Gomes, J. M. P., Parente, A. C. B., Bezerra, J. R., da Costa, M. D. R., Soares, M. S. P., Sampaio, T. L., Lima, F. A. V., et al. (2024) · Metabolic Brain Disease · doi:10.1007/s11011-024-01477-7 · Cited by 8 · see citing works
Algal Elixirs: Unraveling the multifaceted impact of Spirulina in human health
Sharma, R., & Rana, A. R. (2024) · Food Bioscience · doi:10.1016/j.fbio.2024.105365 · Cited by 8 · see citing works
John, U., Patro, N., & Patro, I. K. (2023) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2023.102286 · Cited by 6 · see citing works
Self-citationBo, X. (2025) · The EPMA Journal · doi:10.1007/s13167-025-00405-8 · Cited by 4 · see citing works
Mujtaba, S., Patro, I. K., & Patro, N. (2023) · Brain Sciences · doi:10.3390/brainsci13101360 · Cited by 4 · see citing works
Self-citationBioactive Compounds of the Genus Spirulina Can Prevent the Progression of Neurological Diseases
Elkader, H. A. E. A., Essawy, A. E., & Al‐Shami, A. S. (2024) · Neurochemical Journal · doi:10.1134/s1819712424010057 · Cited by 4 · see citing works
A CMOS Algae Growth Period Monitor for Algaculture Applications
Chiang, C., Nien, C.-Y., Yang, C.-Y., & Chen, S. (2022) · IEEE Sensors Journal · doi:10.1109/jsen.2022.3201429 · Cited by 3 · see citing works
Kambuno, N. T., Putra, A. G. A., Louisa, M., Wuyung, P. E., Timan, I. S., Silaen, O. S. M., Sukria, H. A., & Supali, T. (2025) · Biomedicines · doi:10.3390/biomedicines13020346 · Cited by 3 · see citing works
Sanyoto, D. D., Triawanti, & Noor, M. S. (2021) · IOP Conference Series Earth and Environmental Science · doi:10.1088/1755-1315/913/1/012091 · Cited by 3 · see citing works
Rocha-Gomes, A., Gonçalves, J. S., Veloso, N. C., Ferreira, A. C., Alves, L. T., Rocha, A. C. S., Coimbra, R. L., da Silva, A. D., Pinto, N. A. D., & Riul, T. R. (2026) · European Journal of Neuroscience · doi:10.1111/ejn.70391 · Cited by 2 · see citing works
Kandil, E. H., Samie, H. A. A., AbdElrahman, A. H., & Nofal, A. E. (2024) · Beni-Suef University Journal of Basic and Applied Sciences · doi:10.1186/s43088-024-00543-4 · Cited by 2 · see citing works
Glial Response to Perinatal Multi-Hit Stress: The Triggering Factor for Schizophrenia
Patro, I. K. (2023) · Virology & Immunology Journal · doi:10.23880/vij-16000304 · Cited by 1 · see citing works
Self-citationMujtaba, S., Patro, N., & Patro, I. K. (2025) · Annals of Neurosciences · doi:10.1177/09727531251324716 · Cited by 1 · see citing works
Self-citationThe Glial Perspective of Energy Homeostasis, Neuroinflammation, and Neuro-nutraceuticals
Sinha, S., Patro, N., & Patro, I. K. (2022) · Springer eBooks · doi:10.1007/978-981-16-8313-8_23 · Cited by 1 · see citing works
Self-citationPatro, N., Kushwaha, S. S., & Patro, I. K. (2022) · Springer eBooks · doi:10.1007/978-981-16-8313-8_20
Self-citationPurba, H. H. S., Paramita, R., Prijanti, A. R., & Iswanti, F. C. (2023) · IOP Conference Series Earth and Environmental Science · doi:10.1088/1755-1315/1271/1/012081
Veloso, N. C., Gonçalves, J. S., Rocha‐Gomes, A., Ferreira, A., Alves, L. T., Rocha, A. C. S., Coimbra, R. L., da Silva, A. A., Pinto, N. A. V. D., & Riul, T. R. (2026) · Developmental Psychobiology · doi:10.1002/dev.70166
From Perinatal Stress to Schizophrenia: The Emerging Role of Glial Pathology
Sarkar, T., Patro, N., & Patro, I. K. (2026) · Annals of Neurosciences · doi:10.1177/09727531261445799
Self-citation
- Authors
- Sinha, S., Patro, N., Tiwari, P. K., & Patro, I. K.
- Affiliations
- Jiwaji University (IN)
- Corresponding author
- Patro, Ishan K.
- Venue
- Neurochemistry International
- Publisher
- Elsevier BV
- Published
- 2020-12
- Volume
- 141
- Pages
- 104877
- ISSN
- 0197-0186 (ISSN-L)
- OpenAlex
- W3091792857
- Semantic Scholar
- 0ef297b8f9c878d21709c26f7f553e466127d2d6
- Cited by
- 28
- References
- 119
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 5 · 2022: 7 · 2021: 3 · 2018: 1
- FWCI
- 2.37
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurochemistry International (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Department of Science and Technology, Ministry of Science and Technology, India
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Child Nutrition and Water Access
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
- Keywords
- spirulina supplementation, protein malnutrition, maternal nutrition, pregnancy, lactation, oxidative stress, reactive gliosis, neuronal injury, hippocampus, dendritic spine density, dendritic morphology, apoptosis, F1 progeny, low-protein diet, neuroprotection
- MeSH terms
- Animals, Behavior, Animal, Female, Gliosis, Hippocampus, Lactation, Macrophage Activation, Neuroglia, Neurons, Pregnancy, Protein-Energy Malnutrition, Rats, Sprague-Dawley, Oxidative Stress, Dietary Supplements, Rats, Spirulina
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review