Cited by 501Alzheimer's disease research and treatmentsNeuroinflammation and Neurodegeneration MechanismsDementia and Cognitive Impairment Research

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Intrathecal inflammation precedes development of Alzheimer's disease

Open access

Tarkowski, E·2003·Journal of Neurology, Neurosurgery & Psychiatry

DOI 10.1136/jnnp.74.9.1200PMC PMC1738668

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Abstract

OBJECTIVES: To analyse the cerebrospinal fluid (CSF) values of the proinflammatory cytokines, interleukin 1beta (IL1beta), tumour necrosis factor alpha (TNFalpha), GM-CSF, of the anti-inflammatory cytokine TGFbeta, of tau protein, a marker for neurodegeneration, and of beta amyloid (Abeta), a protein involved in the formation of senile plaques, in prospectively followed up patients with mild cognitive impairment (MCI). METHODS: Analyses of CSF levels of TNFalpha, IL1beta, GM-CSF, TGFbeta, betaa, and tau protein were performed using ELISA in 56 patients with MCI who were followed up prospectively and in 25 age matched, healthy controls. RESULTS: Patients with MCI displayed significantly higher levels of TNFalpha and tau protein and significantly lower levels of TGFbeta and Abeta compared with the healthy controls. After nine months of follow up, 25 patients still displayed MCI while the remaining 31 patients had progressed to Alzheimer's disease (AD). Only MCI patients who progressed to AD at follow up, showed significantly higher CSF levels of TNFalpha than controls. In addition, reduced CSF-Abeta42 levels were only found in MCI patients that progressed to AD, further supporting the notion that disturbed metabolism of Abeta is an early finding in AD. CONCLUSIONS: These results demonstrate increased production of the proinflammatory cytokine, TNFalpha and decreased production of the anti-inflammatory cytokine TGFbeta in patients with MCI at risk to develop AD, suggesting a propensity towards inflammation in this patient group and indicating that CNS inflammation is a early hallmark in the pathogenesis of AD.

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Axonal Protection by 17β-Estradiol through Thioredoxin-1 in Tumor Necrosis Factor-Induced Optic Neuropathy
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The Effect of an Aloe Polymannose Multinutrient Complex on Cognitive and Immune Functioning in Alzheimer's Disease
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Involvement of interleukin‐1 in lipopolysaccaride‐induced microglial activation and learning and memory deficits
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“…of neurodegenerative pathologies such as Alzheimer’s and Parkinson’s diseases (McGeer et al., 1988; Dickson et al., 1993), and it has been shown that TNFa (Tarkowski et al., 2003) and IL1b (Remarque et al., 2001; McGeer and McGeer, 1998) are elevated in the brains of Alzheimer’s disease patients.”
Genetic priming of a proinflammatory profile predicts low IQ in octogenarians
Krabbe, K. S., Mortensen, E. L., Avlund, K., Pilegaard, H., Christiansen, L., Pedersen, B. K., Schroll, M., Jørgensen, T., Pedersen, B. K., & Brüünsgaard, H. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.08.013 · Cited by 33
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Targeting Neuroinflammation as Disease Modifying Approach to Alzheimer’s Disease: Potential and Challenges
Jain, S., Singh, R., Paliwal, S., & Sharma, S. K. (2023) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/1389557523666230511122435 · Cited by 35
Microglia-Derived Interleukin 23: A Crucial Cytokine in Alzheimer's Disease?
Nitsch, L., Schneider, L. H., Zimmermann, J., & Müller, M. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.639353 · Cited by 27
“However, studies of patients with mild cognitive impairment demonstrate neuroinflammation even in the early phase (42, 43).”
Background
Neuroinflammatory profiles regulated by the redox environment predicted cognitive dysfunction in people living with HIV: A cross-sectional study
Spooner, R. K., Taylor, B. K., Moshfegh, C. M., Ahmad, I. M., Dyball, K. N., Emanuel, K. M., Schlichte, S. L., Schantell, M. D., May, P. E., O’Neill, J., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103487 · Cited by 28
Axonal and Cell Body Protection By Nicotinamide Adenine Dinucleotide in Tumor Necrosis Factor-Induced Optic Neuropathy
Kitaoka, Y., Hayashi, Y., Kumai, T., Takeda, H., Munemasa, Y., Fujino, H., Kitaoka, Y., Ueno, S., Sadun, A. A., & Lam, T. T. (2009) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181afecfa · Cited by 29
Tumour necrosis factor induces increased production of extracellular amyloid-β- and α-synuclein-containing aggregates by human Alzheimer’s disease neurons
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“First, increased levels of central and systemic proinflammatory cytokines are observed in mild cognitive impairment and are positively correlated with progression into severe Alzheimer’s disease (Tarkowski et al., 2003; Bermejo et al., 2008).”
Background
A Dichotomous Role for FABP7 in Sleep and Alzheimer’s Disease Pathogenesis: A Hypothesis
Needham, H., Torpey, G., Flores, C. C., Davis, C. J., Vanderheyden, W. M., & Gerstner, J. R. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.798994 · Cited by 29
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p110δ PI3-Kinase Inhibition Perturbs APP and TNFα Trafficking, Reduces Plaque Burden, Dampens Neuroinflammation, and Prevents Cognitive Decline in an Alzheimer's Disease Mouse Model
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“, 1991) and CSF (Tarkowski et al., 2003) of patients with AD, we found that the brain level of TNF was increased in APP/PS1 mice.”
BackgroundInfluential
Effects of a Cyclooxygenase-2 Preferential Inhibitor in Young Healthy Dogs Exposed to Air Pollution: A Pilot Study
Calderón-Garcidueñas, L., Mora-Tiscareño, A., Gómez-Garza, G., Carrasco-Portugal, M. D. C., Pérez-Guillé, B., Flores-Murrieta, F. J., Pérez-Guillé, G., Osnaya, N., Juárez-Olguín, H., Monroy, M. E., et al. (2009) · Toxicologic Pathology · doi:10.1177/0192623309340277 · Cited by 28
Neuroimmune nexus of depression and dementia: Shared mechanisms and therapeutic targets
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Potential long‐term effect of tumor necrosis factor inhibitors on dementia risk: A propensity score matched retrospective cohort study in US veterans
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Alzheimer's disease biomarkers: correspondence between human studies and animal models
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“Inconsistent findings have emerged for measures of alternative cytokines such as tumor necrosis factor-α (TNF-α) and transforming growth factor β (TGF-β) (Blasko et al., 2006; Rota et al., 2006; Tarkowski et al., 2003).”
Background
Mild cognitive impairment (part 2): biological markers for diagnosis and prediction of dementia in Alzheimer's disease
Forlenza, O. V., Diniz, B. S., Teixeira, A. L., Stella, F., & Gattaz, W. F. (2013) · Brazilian Journal of Psychiatry · doi:10.1590/1516-4446-2012-3505 · Cited by 31
Redox Imbalance as a Common Pathogenic Factor Linking Hearing Loss and Cognitive Decline
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“Indeed, increased levels of the proinflammatory cytokine TNF-α and decreased levels of the anti-inflammatory cytokine TNF-β have been found in patients with mild cognitive impairment who progressed to AD [196].”
Background
Astragaloside IV against Alzheimer's disease via microglia-mediated neuroinflammation using network pharmacology and experimental validation
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Progressive Supranuclear Palsy Syndrome: An Overview
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“The notion that neuroinflammation might precede protein aggregation is supported by the higher levels of proinflammatory cytokines such as IL-1 β , TNF-α , and GM CSF in the CSF of patients with mild cognitive impairment (Tarkowski and Andreasen, 2003).”
Background
Curcugreen Treatment Prevented Splenomegaly and Other Peripheral Organ Abnormalities in 3xTg and 5xFAD Mouse Models of Alzheimer’s Disease
Manna, J., Dunbar, G. L., & Maiti, P. (2021) · Antioxidants · doi:10.3390/antiox10060899 · Cited by 26
Ginsenoside compound K acts via LRP1 to alleviate Amyloid β42-induced neuroinflammation in microglia by suppressing NF-κB
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The effects of time-restricted eating on sleep, cognitive decline, and Alzheimer's disease
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“Evidence indicates that inflammation promotes pathological processes that lead to AD (McCaulley and Grush, 2015; Tarkowski et al., 2003).”
Background
Targeting dopamine transporter to ameliorate cognitive deficits in Alzheimer's disease
Shaikh, A., Ahmad, F., Teoh, S. L., Kumar, J., & Yahaya, M. F. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1292858 · Cited by 28
“AD has an intricate pathophysiology that is believed to be initiated by oxidative stress, leading to the deposition of amyloid-β (A β ), tau hyperphosphorylation, neuroinﬂammation, and neurodegeneration (Tarkowski, 2003; Manczak et al., 2011; Leuner et al., 2012).”
Background
Association of the interleukin 1 beta gene and brain spontaneous activity in amnestic mild cognitive impairment
Zhuang, L., Liu, X., Xu, X., Yue, C., Shu, H., Bai, F., Yu, H., Shi, Y., & Zhang, Z. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-263 · Cited by 25
“A case–control study on CSF concluded that intrathecal inflammation precedes the development of AD [41], and found the levels of IL-1β were significantly correlated with the levels of tau and Aβ in”
Background
Extracellular Vesicles Secreted in Response to Cytokine Exposure Increase Mitochondrial Oxygen Consumption in Recipient Cells
Russell, A. E., Jun, S., Sarkar, S., Geldenhuys, W. J., Lewis, S. E., Rellick, S. L., & Simpkins, J. W. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00051 · Cited by 27
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Marcello, A., Wirths, O., Schneider-Axmann, T., Degerman-Gunnarsson, M., Lannfelt, L., & Bayer, T. A. (2009) · Journal of Neural Transmission · doi:10.1007/s00702-009-0224-y · Cited by 25
“However, whether autoimmunity plays a direct role in the patho- genesis of AD is still open to debate (McGeer and McGeer 2001; Singh 1997; Tarkowski et al. 2003).”
Heat Shock Protein 70 and Tumor Necrosis Factor Alpha in Taiwanese Patients with Dementia
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“The cerebrospinal fluid levels of TNF-α were related to cerebral neuronal damage, apoptosis and the clinical variables of dementia. Increased levels of TNF-α were also observed in patients with mild cognitive impairment at risk to develop AD [”
Background
Inverse Relationship Between Alzheimer’s Disease and Cancer: How Immune Checkpoints Might Explain the Mechanisms Underlying Age-Related Diseases
Rogers, N. K., Romero, C., SanMartín, C. D., Ponce, D. P., Salech, F., López, M. N., Gleisner, M. A., Tempio, F., & Behrens, M. I. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-190839 · Cited by 23
Characterisation of amyloid-induced inflammatory responses in the rat retina
Howlett, D. R., Bate, S. T., Collier, S., Lawman, A. J., Chapman, T. D., Ashmeade, T. E., Marshall, I. C. B., Anderson, P. J., Philpott, K. L., Richardson, J. C., et al. (2011) · Experimental Brain Research · doi:10.1007/s00221-011-2819-4 · Cited by 22
“More recent studies using plasma markers as predictors of progression from MCI to AD identified a panel of 18 markers that predicted progression to AD with 90% accuracy (Ray et al. 2007).”
Background
Treatment implications of the altered cytokine-insulin axis in neurodegenerative disease
Clark, I. A., & Vissel, B. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.07.030 · Cited by 23
Diverse pathways to neuronal necroptosis in Alzheimer's disease
Jayaraman, A., & Reynolds, R. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15662 · Cited by 21
“In AD, levels of TNF in the cerebrospinal fluid (CSF) and TNF and TNFR1 protein levels in post-mortem brains have been shown to be increased at an early stage (Hu et al., 2019; Swardfager et al., 2010; Tarkowski et al., 2003; Zhao et al., 2003).”
Background
Mechanisms of abnormal adult hippocampal neurogenesis in Alzheimer’s disease
Zhou, Y., Wang, X., Liu, Y., Gu, Y., Gu, R., Zhang, G., & Lin, Q. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1125376 · Cited by 22
“The activation time of microglia is earlier than that of Aβ and Tau protein pathology in both brains of AD patients and AD mouse models (Tarkowski et al., 2003; Wright et al., 2013).”
Result
Immunity impacts cognitive deficits across neurological disorders
Shaw, B. C., Anders, V., Tinkey, R. A., Habean, M. L., Brock, O. D., Frostino, B. J., & Williams, J. L. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15999 · Cited by 27
Decoding paradoxical links of cytokine markers in cognition: Cross talk between physiology, inflammaging, and Alzheimer’s disease- related cognitive decline
Khan, H., Naseem, T., Kaushik, P., Narang, J., Khan, R., Panwar, S., & Parvez, S. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102535 · Cited by 21
Molecular Regulation Mechanism of Microglial Autophagy in the Pathology of Alzheimer's Disease
Ou-Yang, P., Cai, Z., & Zhang, Z.-H. (2023) · Aging and Disease · doi:10.14336/ad.2023.0106 · Cited by 21
“patients with mild cognitive impairment and AD [3-6], suggesting that intrathecal inflammation precedes AD development.”
Background
Incretin-based therapeutics for the treatment of neurodegenerative diseases
Vear, A., Heneka, M. T., & Clemmensen, C. (2025) · Nature Metabolism · doi:10.1038/s42255-025-01263-4 · Cited by 25
“For example, unlike tau and Aβ 1–42 , levels of the proinflammatory cytokine TNF are elevated in the cerebrospinal fluid (CSF) of people with mild cognitive impairment (MCI) who progress to develop AD compared with that of healthy controls 57 .”
Sleep Disturbance and Alzheimer’s Disease: The Glial Connection
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TNF-α Levels Are Increased in Patients with Subjective Cognitive Impairment and Are Negatively Correlated with β Amyloid-42
Serafini, S., Ferretti, G., Monterosso, P., Angiolillo, A., Costanzo, A. D., & Matrone, C. (2024) · Antioxidants · doi:10.3390/antiox13020216 · Cited by 19
“In this regard, it has previously been found that patients with systemic inflammatory events and elevated plasma TNF-α levels show a 10-fold higher rate of cognitive decline over a 6-month observation period [46,47].”
Background
Mitochondrial Proteome Changes Correlating with β-Amyloid Accumulation
Völgyi, K., Háden, K., Kis, V., Gulyássy, P., Badics, K., Györffy, B. A., Simor, A., Szabó, Z., Janáky, T., Drahos, L., et al. (2016) · Molecular Neurobiology · doi:10.1007/s12035-015-9682-4 · Cited by 20
“TNF level is in good correlation with clinical progression of AD [42].”
Demyelination-derived lysophosphatidylserine promotes microglial dysfunction and neuropathology in a mouse model of Alzheimer’s disease
Zhou, Y., Huang, Z., Lin, B., Ma, M., Hao, Y., Liu, J., Xu, W., Huang, G., Mo, W., Wang, X., et al. (2025) · Cellular and Molecular Immunology · doi:10.1038/s41423-024-01235-w · Cited by 19
Amyloid-β(1−42) Fibrillar Precursors Are Optimal for Inducing Tumor Necrosis Factor-α Production in the THP-1 Human Monocytic Cell Line
Ajit, D., Udan, M. L. D., Paranjape, G. S., & Nichols, M. R. (2009) · Biochemistry · doi:10.1021/bi9003777 · Cited by 18
“Imaging of the Aβ(1-42) aggregation solutions with atomic force microscopy indicated that best cellular response coincided with the appearance of fibrillar structures yet conditions that accelerated or increased Aβ(1-42) fibril formation such as peptide concentration, temperature, or reconstitution in NaOH/PBS at pH 7.”
Influential
Immune Response at the Crossroads of Atherosclerosis and Alzheimer's Disease
Stahr, N. A., & Galkina, E. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.870144 · Cited by 18
“Importantly, elevated TNFα levels and reduced TGFβ production have been detected in the cerebrospinal fluid (CSF) of patients with mild cognitive impairment highlighting that CNS-associated inflammation is an early hallmark in the pathogenesis of AD (31).”
Background
Concentration and proteolysis of CX3CL1 may regulate the microglial response to CX3CL1
Finneran, D. J., Li, Q., Subbarayan, M. S., Joly‐Amado, A., Kamath, S. G., Dengler, D. G., Gordon, M. N., Jackson, M. R., Morgan, D., Bickford, P. C., et al. (2022) · Glia · doi:10.1002/glia.24269 · Cited by 18
“cytokines that have been implicated in neurodegenerative diseases such as PD & AD (Patel et al., 2005; Tarkowski et al., 2003).”
Background
Targeting Progranulin as an Immuno-Neurology Therapeutic Approach
Boylan, M. A., Pincetic, A., Romano, G. J., Tatton, N. A., Kenkare-Mitra, S., & Rosenthal, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242115946 · Cited by 19
Association between disease-modifying antirheumatic drugs for rheumatoid arthritis and risk of incident dementia: a systematic review with meta-analysis
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“25 26 In a double-blind, parallel-group, multicentre trial of 168 patients with early AD, hydroxychloroquine exposure for 18 months showed similar cognitive changes to placebo.”
Background
Involvement of inflammasomes in the pathogenesis of Alzheimer's disease
Beder, N., Belkhelfa, M., & Leklou, H. (2024) · Journal of Alzheimer s Disease · doi:10.1177/13872877241283677 · Cited by 20

Authors: Tarkowski, E.
Affiliations: University of Gothenburg (SE)
Corresponding author: Tarkowski, E
Venue: Journal of Neurology, Neurosurgery & Psychiatry
Publisher: BMJ
Published: 2003-09-01
Volume: 74
Issue: 9
Pages: 1200-1205
ISSN: 0022-3050 (ISSN-L)
DOI: 10.1136/jnnp.74.9.1200
PMC: PMC1738668
OpenAlex: W2071728536
Cited by: 501
References: 53
Citations by year: 2026: 16 · 2025: 17 · 2024: 45 · 2023: 28 · 2022: 43 · 2021: 51 · 2020: 23 · 2019: 30 · 2018: 32 · 2017: 23 · 2016: 18 · 2015: 16 · 2014: 14 · 2013: 13 · 2012: 18
FWCI: 6.52
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neurology Neurosurgery & Psychiatry (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Rune och Ulla Amlövs Stiftelse för Neurologisk och Reumatologisk Forskning
Hjärt-Lungfonden
Göteborgs Läkaresällskap
Svenska Läkaresällskapet
Stiftelsen Konung Gustaf V:s 80-årsfond
Medical Research Council
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Keywords: Alzheimer's disease, mild cognitive impairment, cerebrospinal fluid biomarkers, intrathecal inflammation, inflammatory cytokines, TNF-α, IL-1β, GM-CSF, TGF-beta, tau protein, amyloid-beta, amyloid metabolism, neuroinflammation, disease progression
MeSH terms: Aged, Aged, 80 and over, Alzheimer Disease, Central Nervous System, Cognition Disorders, Female, Humans, Inflammation, Interleukin-1, Male, Middle Aged, Prospective Studies, Risk Factors, Tumor Necrosis Factor-alpha, Granulocyte-Macrophage Colony-Stimulating Factor, Amyloid beta-Peptides, tau Proteins, Plaque, Amyloid

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Intrathecal inflammation precedes development of Alzheimer's disease

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