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Cited by 7Tryptophan and brain disordersEducational Outcomes and InfluencesAdipokines, Inflammation, and Metabolic Diseases

Circulating inflammatory biomarkers and academic performance in adolescents: DADOS study

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Adelantado-Renau, Mireia, Beltran-Valls, Maria Reyes, Mota, Jorge, Moliner-Urdiales, Diego·2020·PLOS ONE
DOI 10.1371/journal.pone.0242016PMC PMC7647075
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Abstract

OBJECTIVE: The present study aimed (1) to examine the association between circulating inflammatory biomarkers and academic performance in adolescents, and (2) to identify the ability of circulating inflammatory biomarkers to predict low academic performance. METHODS: A total of 244 adolescents (13.9±0.3 years, 112 girls) from the DADOS study were included in the analysis. Four inflammatory biomarkers were quantified: white blood cell (WBC) count, interleukin-6, tumor necrosis factor-α (TNF-α), and C-reactive protein (CRP). Academic performance was assessed through academic grades and the Spanish version of the Science Research Associates Test of Educational Abilities. RESULTS: TNF-α was inversely associated with math, Spanish and grade point average (β ranging from -0.166 to -0.124; all p<0.05), while CRP was inversely associated with verbal ability (β = -0.128; p<0.05). Overall, receiver operating characteristic (ROC) curves analyses showed discriminatory ability of WBC and TNF-α in identifying low academic performance (all p<0.05). Moreover, logistic regression analyses indicated that students with levels of WBC and TNF-α above the ROC cut-offs values showed between 78% to 87% increased likelihood of lower academic performance (p<0.05). CONCLUSIONS: Our findings suggested that some circulating inflammatory biomarkers were associated with academic performance in adolescents. Further larger longitudinal and interventional studies are needed to clarify the short-term and long-term relationship between inflammation and academic performance in youths.

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  • Sleep plays a vital role in adolescent health and is directly linked with better academic achievement and physical and mental health.

    “Sleep plays a vital role in the health of adolescents and is directly linked with optimal functioning, including better academic achievement [24][25][26][27] and physical and mental health [28][29][30][31].”

    From Later School Start Times as a Public Health Intervention to Promote Sleep Health in Adolescents (2023) · cites this paper as [24]

    The Introduction and Conclusions discuss inflammatory biomarkers and academic performance, not sleep’s relationship with achievement or physical and mental health. A search for sleep found related study titles in the References, but no passage in this paper reports the claimed links. (LLM, conf=0.76)

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  1. [1]Medzhitov R. Origin and physiological roles of inflammation. Nature. 2008; 454(7203): 428– 35. 10.1038/nature07201 18650913 · DOI · Paper page
  2. [2]Libby P. Inflammation and cardiovascular disease mechanisms. Am J Clin Nutr. 2006; 83(2): 456S– 460S. 10.1093/ajcn/83.2.456S 16470012 · DOI
  3. [3]Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006; 444(7121): 860– 7. 10.1038/nature05485 17167474 · DOI · Paper page
  4. [5]McAfoose J, Baune BT. Evidence for a cytokine model of cognitive function. Neurosci Biobehav Rev. 2009; 33(3): 355– 66. 10.1016/j.neubiorev.2008.10.005 18996146 · DOI · Paper page
  5. [6]Kyriklaki A, Margetaki K, Kampouri M, Koutra K, Bitsios P, Chalkiadaki G, et al Association between high levels of inflammatory markers and cognitive outcomes at 4 years of age: The Rhea mother-child cohort study, Crete, Greece. Cytokine. 2019; 117: 1– 7. 10.1016/j.cyto.2019.01.010 30772773 PMC8801160 · DOI
  6. [7]Kuban KCK, Joseph RM, O’Shea TM, Heeren T, Fichorova RN, Douglass L, et al Circulating Inflammatory-Associated Proteins in the First Month of Life and Cognitive Impairment at Age 10 Years in Children Born Extremely Preterm. J Pediatr. 2017; 180: 116– 123.e1. 10.1016/j.jpeds.2016.09.054 27788929 PMC5183478 · DOI
  7. [8]Rose J, Vassar R, Cahill-Rowley K, Hintz SR, Stevenson DK. Neonatal Biomarkers of Inflammation: Correlates of Early Neurodevelopment and Gait in Very-Low-Birth-Weight Preterm Children. Am J Perinatol. 2015; 33(1): 71– 8. 10.1055/s-0035-1557106 26212060 · DOI
  8. [9]Frodl T, Amico F. Is there an association between peripheral immune markers and structural/functional neuroimaging findings? Prog Neuro-Psychopharmacology Biol Psychiatry. 2014; 48: 295– 303. 10.1016/j.pnpbp.2012.12.013 23313563 · DOI
  9. [10]Sartori AC, Vance DE, Slater LZ, Crowe M. The impact of inflammation on cognitive function in older adults: implications for healthcare practice and research. J Neurosci Nurs. 2012; 44(4): 206– 17. 22743812 PMC3390758
  10. [12]Cullen AE, Tappin BM, Zunszain PA, Dickson H, Roberts RE, Nikkheslat N, et al The relationship between salivary C-reactive protein and cognitive function in children aged 11–14 years: Does psychopathology have a moderating effect? Brain Behav Immun. 2017; 66: 221– 9. 10.1016/j.bbi.2017.07.002 28694011 PMC5773474 · DOI
  11. [13]Jonker I, Klein HC, Duivis HE, Yolken RH, Rosmalen JGM, Schoevers RA. Association between Exposure to HSV1 and Cognitive Functioning in a General Population of Adolescents. The TRAILS Study. Morton JB, editor. PLoS One. 2014; 9(7): e101549 10.1371/journal.pone.0101549 24983885 PMC4077793 · DOI
  12. [14]Lê-Scherban F, Diez Roux AV, Li Y, Morgenstern H. Does academic achievement during childhood and adolescence benefit later health? Ann Epidemiol. 2014; 24(5): 344– 55. 10.1016/j.annepidem.2014.02.008 24792585 PMC4037140 · DOI · Paper page
  13. [16]Esteban-Cornejo I, Martinez-Gomez D, Gómez-Martínez S, del Campo-Vecino J, Fernández-Santos J, Castro-Piñero J, et al Inflammatory biomarkers and academic performance in youth. The UP & DOWN Study. Brain Behav Immun. 2016; 54: 122– 7. 10.1016/j.bbi.2016.01.010 26778777 · DOI
  14. [17]Adelantado-Renau M, Beltran-Valls MR, Esteban-Cornejo I, Martínez-Vizcaíno V, Santaliestra-Pasías AM, Moliner-Urdiales D. The influence of adherence to the Mediterranean diet on academic performance is mediated by sleep quality in adolescents. Acta Paediatr Int J Paediatr. 2019; 108(2): 339– 346. 10.1111/apa.14472 30019348 · DOI
  15. [20]Correa-Burrows P, Rodriguez Y, Blanco E, Gahagan S, Burrows R. Increased adiposity as a potential risk factor for lower academic performance: A cross-sectional study in Chilean adolescents from low-to-middle socioeconomic background. Nutrients. 2018; 10(9): 1133 10.3390/nu10091133 30134573 PMC6165189 · DOI
  16. [21]Al-Domi H, Al-Shorman A. Increased waist circumference is associated with subclinical atherosclerosis in schoolchildren. Diabetes Metab Syndr Clin Res Rev. 2019; 13(1): 264– 9. 10.1016/j.dsx.2018.09.004 30641709 · DOI
  17. [22]Schwingshackl L, Hoffmann G. Mediterranean dietary pattern, inflammation and endothelial function: A systematic review and meta-analysis of intervention trials. Nutr Metab Cardiovasc Dis. 2014; 24(9): 929– 39. 10.1016/j.numecd.2014.03.003 24787907 · DOI
  18. [23]Tanner JM, Whitehouse RH. Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child. 1976; 51(3): 170– 9. 10.1136/adc.51.3.170 952550 PMC1545912 · DOI · Paper page
  19. [24]Vukojević M, Zovko A, Talić I, Tanović M, Rešić B, Vrdoljak I, et al Parental socioeconomic status as a predictor of physical and mental health outcomes in children—Literature review. Acta Clin Croat. 2017; 56(4): 742– 8. 10.20471/acc.2017.56.04.23 29590731 · DOI
  20. [25]Adelantado-Renau M, Diez-Fernandez A, Beltran-Valls MR, Soriano-Maldonado A, Moliner-Urdiales D. The effect of sleep quality on academic performance is mediated by Internet use time: DADOS study. J Pediatr (Rio J). 2019; 95(4): 410– 418. 10.1016/j.jped.2018.03.006 29787701 · DOI · Paper page
  21. [26]Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ. 2000; 320(7244): 1240– 3. 10.1136/bmj.320.7244.1240 10797032 PMC27365 · DOI
  22. [27]Serra-Majem L, Ribas L, Ngo J, Ortega RM, García A, Pérez-Rodrigo C, et al Food, youth and the Mediterranean diet in Spain. Development of KIDMED, Mediterranean Diet Quality Index in children and adolescents. Public Health Nutr. 2004; 7(07): 931– 5. 15482620
  23. [28]Marsland AL, Gianaros PJ, Kuan DCH, Sheu LK, Krajina K, Manuck SB. Brain morphology links systemic inflammation to cognitive function in midlife adults. Brain Behav Immun. 2015; 48(April): 195– 204. 10.1016/j.bbi.2015.03.015 25882911 PMC4508197 · DOI · Paper page
  24. [29]Grigoleit J-S, Oberbeck JR, Lichte P, Kobbe P, Wolf OT, Montag T, et al Lipopolysaccharide-induced experimental immune activation does not impair memory functions in humans. Neurobiol Learn Mem. 2010; 94(4): 561– 7. 10.1016/j.nlm.2010.09.011 20875866 · DOI · Paper page
  25. [30]Artero EG, España-Romero V, Jiménez-Pavón D, Martinez-Gómez D, Warnberg J, Gómez-Martínez S, et al Muscular fitness, fatness and inflammatory biomarkers in adolescents. Pediatr Obes. 2014; 9(5): 391– 400. 10.1111/j.2047-6310.2013.00186.x 23828843 · DOI
  26. [31]Pérez de Heredia F, Garaulet M, Gómez-Martínez S, Díaz LE, Wärnberg J, Androutsos O, et al Self-reported sleep duration, white blood cell counts and cytokine profiles in European adolescents: The HELENA study. Sleep Med. 2014; 15(10): 1251– 8. 10.1016/j.sleep.2014.04.010 25156749 · DOI · Paper page
  27. [32]Lee SE, West KP, Cole RN, Schulze KJ, Wu LS-F, Yager JD, et al General intelligence is associated with subclinical inflammation in Nepalese children: A population-based plasma proteomics study. Brain Behav Immun. 2016; 56: 253– 63. 10.1016/j.bbi.2016.03.023 27039242 PMC4929134 · DOI
  28. [33]Windham BG, Simpson BN, Lirette S, Bridges J, Bielak L, Peyser PA, et al Associations between inflammation and cognitive function in African Americans and European Americans. J Am Geriatr Soc. 2014; 62(12): 2303– 10. 10.1111/jgs.13165 25516026 PMC4270090 · DOI

Authors
Adelantado-Renau, M., Beltran-Valls, M. R., Mota, J., & Moliner-Urdiales, D.
Affiliations
Universidade do Porto (PT)
ORCID
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2020-11-06
Volume
15
Issue
11
Pages
e0242016
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0242016
PMC
PMC7647075
OpenAlex
W3097401595
Cited by
7
References
4
Citations by year
2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2021: 1
FWCI
0.15
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Repositori UJI (Universitat Jaume I) (publishedVersion, other-oa)
  • LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-sa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Ministerio de Economía y Competitividad (DEP2013-45515-R)
  • Universitat Jaume I (P1·1A2015-05, UJI-A2019-12, E-2018-21)
  • Fundo Regional para a Ciência e Tecnologia (SFRH/BSAB/142983/2018, UID/DTP/00617/2019)
  • Schweppes Suntory Spain (Sunny Sport research grant 2015)
  • Fundación Banco Santander (Programa de Bolsas Santander Universidades 2018)
Topics
  • Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
  • Social Sciences › Education › Educational Outcomes and Influences
  • Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
Keywords
inflammatory markers, academic performance, adolescents, TNF-α, C-reactive protein, interleukin-6, white blood cell count, verbal ability, mathematical ability
MeSH terms
Academic Performance, Adolescent, C-Reactive Protein, Female, Humans, Inflammation, Leukocyte Count, Male, ROC Curve, Tumor Necrosis Factor-alpha, Biomarkers, Interleukin-6

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