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Traverso, Annalisa (2018) Brain-Derived Neurotrophic Factor (BDNF) and IL-1beta in Pediatric and Adolescent' Depressive Disorders: a look towards precision psychiatry. [Ph.D. thesis]

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Abstract (italian or english)

Introduction. Depression is one of the main and most debilitating mood disorders, as for personal functioning and social costs (Masi and Brovedani, 2011). It is estimated that depression affects more than 15% of the population lifetime (Kessler et al., 2003), with percentages in pediatric age that reach about 1-2% in prepuberal age and 4-6% in adolescence (Kessler et al., 2001). Although the early-onset depression usually tends to improve over time and resolve in a part of the cases, the functional impact of the disease is more difficult to recover, with consequences that tend to take a chronic trend and finally predispose to a high rate of recurrence of disease, a high risk of psychopathology in the future, as well as increase risk of suicide attempts and completed suicides (Masi and Brovedani, 2011). Studies on neuroanatomy, post-mortem brain observations and in vivo neuroimaging suggest that the impairment of neuroplasticity in specific neuronal networks may be involved in the pathogenesis of mood disorders (Biggio, 2011). In particular, recent studies have emphasized the role of the neurotrophic factor called Brain Derived Neurotrophic Factor (BDNF) whose depletion is associated with a reduction in neurogenesis and in the volume of important brain areas including the hippocampus, the prefrontal cortex and the amygdala (Biggio, 2011). Other researches found reduced BDNF concentrations in the blood of depressed patients, which increased after undergoing treatment with psychopharmacological therapy (Brunoni et al., 2008; Sen et al., 2008; Bocchio-Chiavetto et al., 2010; Molendijk et al. al., 2014). Scientific studies also found that the neuroinflammation process could contribute to the origin of some psychiatric conditions, especially depression (Dantzer et al. 2008; Miller et al. 2009; Kim et al. 2014; Rosenblat et al. 2014). Depressed patients often present an increase levels of proinflammatory cytokines (like IL-1beta) in blood and cerebrospinal fluid (Miller et al, 2009; Kim et al. 2014), so many authors have hypothesized their role as early clinical biomarker of pathology.
Objective. The aim of the present study is to measure plasma levels of BDNF and IL-1beta in subjects affected by depression in the developmental age compared to healthy peers. Secondary aims are: a) the evaluation in the depressed subjects of the trend of plasma levels before and after psychopharmacological treatment (at 3, 6 and 12 months); b) the analysis of the relationship between plasma levels of BDNF and IL-1beta and clinical psychopatological features of depression. The last objective is to verify the usefulness of BDNF and IL-1beta dosages as peripheral biomarkers of disease or of unresponsiveness to treatment, finally to improve diagnostic characterization of depressed patients and to target the treatment in pediatric age.
Methods. Thirteen subjects aged 11-17,9 years, diagnosed with depressive disorder (according to DSM-IV-TR; APA, 2002), as well as matched healthy subjects (n =12), were evaluated by trained raters and provided blood for BDNF and IL-1beta measurements.
The diagnostic evaluation was conducted through free talks and the administration of a panel of structured (YSR-CBCL, CDI, MASC, CGI, C-GAS, SadPerson) and projective tests. The same panel was adminstrated to healthy subjects to explore subthereshold dimensions. Depressed subjects were treated with pharmacological therapy (Selective Serotonin Reuptake Inhibitors, mood stabilizers, SGAs) and psychotherapy.
The plasma levels of BDNF and IL-1beta were measured according to definite timing (basal T0, before the start of therapy / psychotherapy, after 6 and 12 months). For depressed patients, an additional measure after 3 months of therapy was performed.
Analysis of BDNF and IL-1beta levels were performed using specific ELISA kits (BDNF Emax ImmunoAssay System, Promega, Madison, U.S.A and Antigenix America, Huntington Station, NY, USA)
Results. The depressed subjects, compared to the healthy peers, differ in a statistically significant way for a constant familiarity for psychiatric pathology, in particular in the maternal line, a history of events experienced as traumatic, a constant presence of conflicts within the family, scholastic and relational problems, sleep disorders and alcohol/drugs use. Compared to heathy subjects at intake, plasma BDNF concentrations are lower, while IL-1beta are higher in depressed patients, even if they do not reach a statistical significance. Regarding psychodiagnostic assessment, comparing test scores between depressed and non-depressed subjects at T0, there are significant differences in CBCL, YSR, C-GAS, CGI-S, CDI (p <0.05) and SadPerson (p <0.001) scores. No significant differences were found between the gropus in the MASC scores. Statistically significant correlations were found between BDNF levels at T0 of depressed subjects and problems of attention (r=-.695, p=.026) and school skills (r= .878, p= .004). At T6, BDNF inversely correlates to affective disorders (r=-.975, p=.005) reported at YSR T12. In depressed group, considering the presence of suicidal attempts, there are statistical significative differences for anxious-depressed (Z=-2.158, p=.031) and anxiety problems (Z=-2.669, p=.008) at YSR. The same analysis performed considering the personal history of trauma, highlighted statistical significative differences for rule break (Z=-2.384, p=.017) and conduct disorders (Z=-2.037, p=.042).
Conclusions. Depressed pediatric patients present lower levels of BDNF and higher levels of IL-1beta compared to healthy peers at the moment of diagnosis, although without a statistical significant difference. At intake BDNF appears to correlate to academic competences, while after 6 months of therapy higher BDNF levels orient to a better prognosis as for depression symptomatology. The evolution from suicidal ideation to SA appear to be linked to the perception of limited social support (reduced resilience) in adolescents with reduced levels of BDNF.
Depressed children with a history of trauma present more externalizing symptoms, while the dimension of anxiety appears to be somehow protective from suicidal attempts.
The study supports the bio-psycho-social model of DD, highlighting the importance of a balance between neurogenesis, neuroinflammation and cerebral plasticity in the delicate period of developmental age. BDNF seems to be a symptoms or disease biomarker more than a severity index, so the integration of different instruments of evaluations, both clinical and biological (multimodal methods), as well as the integration of different voices (multi-informant approach) seems to represent the “best practice” for pediatric clinical assessment of mental health in line with precision psychiatry.
Further studies are needed to explore the role of BDNF and cytokines in the response of pediatric population to SSRIs, to identify biomarkers for predicting early treatment response, to produce new drug targets, to find preventive strategies and individually target therapy.

Abstract (a different language)

Introduzione. La depressione è uno tra i principali e maggiormente debilitanti disturbi dell'umore, sia in termini di funzionamento personale che di costi sociali (Masi and Brovedani, 2011). Si stima che la depressione colpisca almeno una volta nella vita più del 15% della popolazione (Kessler et al., 2003), con percentuali in età pediatrica che raggiungono circa l’1-2% in epoca prepuberale e il 4-6% nell’adolescenza (Kessler et al., 2001). Nonostante la depressione ad esordio precoce solitamente tenda a migliorare nel tempo e a risolversi in una parte dei casi, l’impatto funzionale della malattia risulta più difficile da recuperare, con conseguenze che tendono ad assumere un andamento cronico e che infine predispongono ad un alto tasso di ricorrenza di malattia, un alto rischio di psicopatologia futura, tentativi di suicidio e suicidi completati (Masi et Brovedani,2011).
Studi di neuroanatomia, osservazioni condotte sul cervello post-mortem e ricerche di neuroimaging in vivo suggeriscono che la compromissione della neuroplasticità a livello di specifiche reti neuronali possa essere coinvolta nella patogenesi dei disturbi dell’umore (Biggio, 2011). In particolare, studi recenti hanno sottolineato il ruolo di un fattore neurotrofico denominato Brain Derived Neurotrophic Factor (BDNF) la cui deplezione è associata a riduzione della neurogenesi e del volume di importanti aree cerebrali tra cui l’ippocampo, la corteccia prefontale e l’amigdala (Biggio, 2011). Altre ricerche hanno riscontrato concentrazioni ridotte di BDNF nel sangue di pazienti depressi e un successivo incremento a seguito di trattamento con terapia psicofarmacologica (Brunoni et al., 2008; Sen et al., 2008; Bocchio-Chiavetto et al., 2010; Molendijk et al., 2014). Altri studi scientifici evidenziano che anche processi di neuroinfiammazione possono contribuire all'origine di alcune patologie psichiatriche ed in particolar modo della depressione (Dantzer et al. 2008; Miller et al.2009; Kim et al. 2014; Rosenblat et al. 2014). I pazienti depressi infatti presentano spesso aumenti dei livelli di citochine proinfiammatorie (come l'IL-1beta) nel sangue e nel liquor (Miller et al, 2009; Kim et al. 2014), pertanto molti autori ipotizzano un loro ruolo come biomarker precoci di malattia.
Scopo dello studio. Lo scopo dello studio è la misurazione dei livelli plasmatici di BDNF e di IL-1beta in soggetti affetti da depressione in età evolutiva rispetto ad un gruppo di soggetti sani. Obiettivi secondari sono: a) la valutazione nei soggetti depressi dell'andamento dei livelli plasmatici prima e dopo trattamento psicofarmacologico (a 3, 6 e 12 mesi); b) la valutazione della relazione tra livelli plasmatici di BDNF e IL-1beta e le caratteristiche cliniche psicopatologiche della depressione. Obiettivo finale è verificare l'utilità del dosaggio del BDNF e dell'IL-1beta, quali possibili biomarkers periferici di malattia o di mancata risposta alla terapia, per migliorare la caratterizzazione dei pazienti depressi e finalizzare il trattamento in età pediatrica.
Materiali e metodi. Tredici soggetti di età compresa tra 11 e 17,9 anni, con diagnosi di disturbo depressivo (secondo il DSM-IV-TR, APA, 2002), e un parallelo gruppo di soggetti sani appaiati per sesso ed età (n = 12), sono stati valutati da personale specializzato. Sono stati prelevati inoltre campioni ematici per la misurazione di BDNF e IL-1beta. La diagnosi è stata condotta attraverso colloqui liberi e la somministrazione di test strutturati (YSR-CBCL, CDI, MASC, CGI, C-GAS, SadPerson) e proiettivi. Gli stessi test sono stati somministrati anche ai soggetti sani per esplorare la presenza di eventuali dimensioni depressive sottosoglia. I soggetti depressi sono stati trattati con terapia farmacologica (inibitori selettivi della ricaptazione della serotonina, stabilizzatori dell'umore, antipsicotici atipici) e psicoterapia. I livelli plasmatici di BDNF e IL-1beta sono stati misurati secondo tempi definiti (T0 basale, prima dell'inizio della terapia/ psicoterapia, dopo 6 e 12 mesi). Per i pazienti depressi, è stata eseguito un ulteriore dosaggio dopo 3 mesi di terapia. L'analisi dei livelli di BDNF e IL-1beta è stata eseguita utilizzando specifici kit ELISA (BDNF Emax ImmunoAssay System, Promega, Madison, U.S.A and Antigenix America, Huntington Station, NY, USA)
Risultati. I soggetti depressi, rispetto ai coetanei sani, differiscono in modo statisticamente significativo per una costante familiarità per la patologia psichiatrica, in particolare in linea materna, una anamnesi positiva per traumi, una costante presenza di conflitti all'interno della famiglia, problemi scolastici e relazionali, disturbi del sonno e uso di alcol o sostanze. Rispetto ai soggetti sani, al momento del reclutamento, le concentrazioni plasmatiche di BDNF nei pazienti depressi risultano più basse, mentre quelle di IL-1beta più alte, tuttavia i risultati non raggiungono una significatività statistica.
Per quanto riguarda la valutazione psicodiagnostica, confrontando i punteggi dei test tra soggetti depressi e non depressi a T0, vi sono differenze significative nei punteggi delle CBCL, YSR, C-GAS, CGI-S, CDI (p <0,05) e SadPerson (p <0,001). Nessuna differenza significativa è stata trovata tra i gruppi nei punteggi MASC. Nei soggetti con depressione è presente una correlazione statisticamente significativa tra i livelli di BDNF al T0 e problemi di attenzione (r = -. 695, p = 0,026) e abilità scolastiche (r = .878, p = 0,004). A T6, i livelli di BDNF sono inversamente correlati a disturbi affettivi (r = -. 975, p = 0,005) riportati al test YSR a 12 mesi. Nel gruppo di soggetti depressi, considerando la presenza di tentativi di suicidio, esistono differenze statisticamente significative per problemi ansioso/depressivi (Z = -2,158, p = 0,031) e di ansia (Z = -2,669, p = 0,008) riportati al YSR. La stessa analisi eseguita considerando l'anamnesi positiva per eventi traumatici, ha evidenziato differenze statisticamente significative per lo scarso rispetto delle regole (Z = -2.384, p = .017) e i disturbi del comportamento (Z = -2.037, p = .042).
Conclusioni. I pazienti pediatrici depressi presentano livelli più bassi di BDNF e livelli più alti di IL-1beta rispetto ai coetanei sani al momento della diagnosi, sebbene il dato non raggiunga una differenza statisticamente significativa. Al momento del reclutamento, il livello di BDNF appare correlare con le competenze accademiche, mentre dopo 6 mesi di terapia livelli di BDNF più elevati orientano verso una prognosi migliore relativamente alla sintomatologia depressiva. L'evoluzione dall'ideazione suicidaria al tentato suicidio sembra essere collegata alla percezione di un limitato supporto sociale (ridotta resilienza) negli adolescenti con livelli ridotti di BDNF. I bambini depressi con una storia di trauma presentano sintomi più esternalizzanti, mentre la dimensione dell'ansia sembra essere in qualche modo protettiva rispetto al tentativo di suicidio.
Lo studio supporta il modello bio-psico-sociale dei DD, evidenziando l'importanza di un equilibrio tra neurogenesi, neuroinfiammazione e plasticità cerebrale nel delicato periodo dell’età evolutiva. Il BDNF sembra essere un biomarcatore di sintomi e di patologia, piuttosto che un indice di gravità, pertanto l'integrazione di diversi strumenti di valutazione, sia clinici che biologici (metodi multimodali), così come l'integrazione di diverse voci (approccio multi-informant) sembrano rappresentare la "migliore pratica" per la valutazione clinica pediatrica della salute mentale in linea con la psichiatria di precisione.
Ulteriori studi si rendono necessari al fine di esplorare il ruolo del BDNF e delle citochine nella risposta terapeutica agli SSRI nella popolazione pediatrica, per identificare biomarkers predittori precoci di risposta al trattamento, per la produzione di nuovi bersagli farmacologici, per trovare strategie preventive e mirare ad una terapia individualizzata nella depressione.

EPrint type:Ph.D. thesis
Tutor:Battistella, Pier Antonio
Ph.D. course:Ciclo 31 > Corsi 31 > MEDICINA DELLO SVILUPPO E SCIENZE DELLA PROGRAMMAZIONE SANITARIA
Data di deposito della tesi:28 November 2018
Anno di Pubblicazione:28 November 2018
Key Words:depressione pediatrica, BDNF, IL-1beta, psichiatria di precisione, età evolutiva, pediatric depression, BDNF, IL-1beta, precision psychiatry, developmental age
Settori scientifico-disciplinari MIUR:Area 06 - Scienze mediche > MED/39 Neuropsichiatria infantile
Struttura di riferimento:Dipartimenti > Dipartimento di Salute della Donna e del Bambino
Codice ID:11435
Depositato il:06 Nov 2019 12:04
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