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Lodi, Alessandra (2017) Effects of a ketogenic mediterranean diet on physiological and psychological variables. [Ph.D. thesis]

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Abstract (english)

Ketogenic diets (KDs) are diets in which the net carbohydrate intake, calculated by subtracting fibres from total carbohydrates, is between 20 and 50 g/day (<10% of total energy intake) with a variable proportion of proteins and fats (Noakes, Windt 2017). In these conditions, glycogen stores are depleted (Paoli, Canato et al. 2011), insulin level is low and energy metabolism is mainly dependent from fat oxidation. KDs lead a significant increase in circulating levels of ketone bodies (KBs) β-hydroxybutyrate (βOHB), acetoacetate (AcAc) and acetone (Veldhorst, Westerterp et al. 2010). While AcAc and βOHB are used as energy, acetone is a volatile compound and is eliminated through expiration, giving the “sweet” breath odour typical of ketosis, or via renal excretion (Paoli, Canato et al. 2011). The concentration of KBs in the blood of healthy individuals during the carbohydrate fed state is about 0.1 mmol/L and increases to about 0.3 mmol/L after an overnight fast, but after prolonged fasting up to 20 days KBs can increase to more than 10 mmol/L. A diet is considered “ketogenic” when produces a stable increase in the level of βOHB higher than 0.6 mmol/L (Wiggam, O'Kane et al. 1997) or when the molar ratio of blood glucose to blood ketone body βOHB is less than or equal to 1 (Meidenbauer, Mukherjee et al. 2015). Since KBs AcAc and βOHB are acids, the ketosis state implies a condition of acidosis. Given the fact that the pH of the blood is 7.4 and that the pKa of AcAc is 3.8 and that of βOHB is 4.8, these acids circulate in the blood in a completely dissociated form and are eliminated together with sodium and potassium ions (Siliprandi & Tettamanti 2011). This loss of cations implies a decrease of pH, which is normally balanced from the body apart when potassium and sodium intake are impaired (Phinney 2004) or in pathological overproduction of KBs during untreated diabetes type 1 which leads to diabetic ketoacidosis, characterized by a KBs level higher than 20 mmol/L with a decrease of pH. Biochemistry Hans Krebs was the first who diversified physiologic from pathologic ketosis (Krebs 1966). For skeletal and cardiac muscle, which usually oxidize fats, the use of KBs is a relative advantage, while for the central nervous system, in which the entrance of fatty acids is prevented from the blood-brain-barrier (BBB), the availability of KBs is an important surrogate of glucose, which is the habitual substrate of nervous tissue. During starvation, under a ketogenic diet or in new-born infants, the brain can utilize KBs as primary fuel instead of glucose (Laeger, Metges et al. 2010) in proportion to the degree of ketosis (Hartman, Gasior et al.). βOHB is the most abundant circulating ketone body and its transport across the blood-brain barrier is mediated both by diffusion and by several monocarboxylic acid transporters as MCT1 and MCT2, the former being upregulated during a ketogenic diet (Newman, Verdin 2014). This complementary action between the liver, which produces KBs in periods of shortage of carbs, and the CNS which use them, it’s a very important event which was determinant for the survival of the human species over the millennia.

My research focused on three important aspects of KDs and weight loss, which needed further investigation:
1. long-term successful weight loss after a KD: the maintenance of weight loss over long time is challenging and the fear of weight regain is common, so that this phenomenon is named “yo-yo” effect. In this regard, low-carbohydrate diets are known to bring better results compared to low-fat diets in terms of weight loss (Shai, Schwarzfuchs et al. 2008) but not of compliance (Greenberg, Stampfer et al. 2009). Recently, Sumithran and colleagues have demonstrated that the increase in circulating ghrelin and in subjective appetite, which accompanied a hypocaloric diet, was reduced with a ketogenic approach (Sumithran, Prendergast et al. 2013). Thus, we hypothesized that certain aspects of the KD such as muscle mass retention, RMR (resting metabolic rate) and orexigenic hormone stability combined with the acknowledged health benefits of traditional Mediterranean nutrition may favour long-term weight loss. The aim of our study was to investigate the effect on weight and body composition of two short periods of a modified KD, i.e., a very low carbohydrate ketogenic diet with phytoextracts (KEMEPHY) (Paoli, Cenci et al. 2010, Paoli 2011, Paoli 2012) interspersed between longer periods of maintenance nutrition, based on the traditional Mediterranean diet, over a total period of 12 months in obese/overweight healthy subjects and was designed as a retrospective study. We analysed 89 male and female subjects, aged between 25 and 65 years who were overall healthy apart from being obese (mean BMI 35.82 ± 4.11 kg/m2). Data from this study demonstrate that the majority of subjects showed significant weight loss (10%) as a result of a two-phase KD and were compliant both during the six month weight loss phase and the six month normocaloric maintenance phase, with no weight regain. Moreover, the proposed protocol led improvements in health risk factors (total cholesterol, LDL cholesterol, triglycerides and glucose levels) in the majority of subjects. Compliance was very high which was a key determinant of the results seen;
2. formulation of new low-carbohydrate ultraprocessed foods to overcome the lack of sweet taste during a KD: a point of interest, which has always been a detrimental aspect of KDs, is the lack of sweet taste, which could be difficult to sustain for long periods, especially for people with a high sweet food preference. During consumption of a KD, it is mandatory to maintain a low level of glycaemia (about 80–90 mg/dL) to avoid insulin spikes (Paoli, Canato et al. 2011). This condition allows subjects to improve their fat oxidation as demonstrated by Paoli et al. (Paoli, Grimaldi et al. 2012) and by Tagliabue et al. (Tagliabue, Bertoli et al. 2012). Today the new food technology, which is able to build ultra-processed products very low in sugar content and high in protein and fibres, can help to solve this problem, formulating products with a high palatability and ready-to-consume format, useful both in ketosis and in easier low carb diets. Usually, ultra-processed products lack in proteins and fibres and produce postprandial glucose and insulin spikes (PAHO WHO 2015). This effect is known to elicit food craving and overeating, with a preference for high-glycaemic index carbohydrates (high-GI CHO) (Lennerz, Alsop et al. 2013), a phenomenon defined as CHO-craving effect (Ventura, Santander et al. 2014). In order to analyse the effect of 10 different high-protein low-CHO proprietary foods on glycaemia, we recruited 14 healthy females, which were tested for their glycaemic response through the glycaemic score (GS) method. All test foods, compared with glucose, produced a significantly lower glycaemic response and their GS resulted lower than 25 (compared to the reference GS value of glucose which is 100). We concluded that the reformulation of ultraprocessed ready-to-consume foods in a low-CHO, high-protein version can produce a significantly lower glycaemic response whilst maintaining the valued ready-to-use format and high palatability demanded by consumers, facilitating the adherence to a KD of individuals who tend to have a high preference for sweet foods;
3. effect of KDs on cognitive functions: the range of variation of glucose and ketone bodies (KBs) in the blood of non-diabetic individuals is wide and both of them can be used as energy from the brain. Data on glycaemia and ketonemia effects on cognitive functions on healthy humans following different diets are scarce. The purpose of this study was then to compare the effects of glycaemia and ketonemia variation after ten days of two different ketogenic diets and a calorie-restricted Mediterranean diet (MD) on working memory and executive functions in 63 sedentary healthy overweight (BMI>25) young women (age: 20-35), which were recruited in the university area. Subjects were divided in groups according to the day of the beginning of their follicular phase in order to minimize hormonal effects on mood and came for the basal measurements five days before the start of the dietary protocol. The following controls were set on the starting day of the diet (t1), on the third (t3), on the fifth (t5), on the seventh (t7) and on the last day (t10). On the basal control day, the weight of the subjects was measured and a body impedance analysis was performed. Subjects took a standard high carb breakfast and afterwards they completed the psychological tests. At t1, t3, t5, t7 and t10 ketone bodies levels and glycaemia were measured, as well as appetite levels. On the last control day (t10) subjects repeated the body impedance analysis, the body weight measure and, after breakfast (each group had a different breakfast according to the prescribed diet), the psychological tests. Psychological tests consisted in a mood test, two cognitive tasks, one to investigate working memory (visuo-spatial n back) and the second to stress executive functions (inhibitory control task) and in a VAS scale to test the appetite level. 45 subjects completed the study. Considering all participants together, pre-diet glucose levels were positively correlated with reaction time in the go-trial of the executive function test (r(43) = 0.358, p = 0.018), but this relation was not found in the post-diet measure both when subjects were analysed all together and when subjects were divided according to the type of diet followed. In the same psychological test, in the post-diet measure ketonemia showed a negative correlation with accuracy of the no-go trials (r(29) = -0.455, p = 0.027). We can conclude that healthy young overweight subjects with fasting glycaemia below prediabetes level were negatively affected by a high-carb breakfast during an executive function test. Moreover, the effect of mild KBs levels (2 ± 1.3 mmol/L) negatively affected accuracy of the no-go trials of the executive functions test.

Abstract (italian)

Le diete chetogeniche sono diete in cui l’introito netto di carboidrati, calcolato sottraendo la quantità di fibre dai carboidrati totali, è tra 20 e 50 g/gg (<10% dell’apporto energetico totale) con una proporzione variabile di proteine e grassi (Noakes, Windt 2017). In queste condizioni le riserve di glicogeno sono esaurite (Paoli, Canato et al. 2011), il livello di insulina è basso e il metabolismo energetico dipende prevalentemente dall’ossidazione dei grassi. Le diete chetogeniche portano un aumento significativo dei livelli circolanti dei corpi chetonici β-idrossibutirrato, acetoacetato e acetone (Veldhorst, Westerterp et al. 2010). Mentre sia l’acetoacetato che il β-idrossibutirrato vengono utilizzati come energia, l’acetone è volatile ed è eliminato attraverso l’espirazione, dando all’alito quella nota “fruttata” tipica della chetosi, oppure attraverso i reni (Paoli, Canato et al. 2011). La concentrazione ematica dei corpi chetonici in individui sani che seguono una dieta costituita prevalentemente da carboidrati è 0,1 mmol/L e può salire fino a 0,3 mmol/L dopo il digiuno notturno, ma dopo venti giorni di digiuno il livello di corpi chetonici può salire oltre 10 mmol/L. Una dieta è considerata “chetogenica” quando produce un aumento del livello di β-idrossibutirrato superiore a 0,6 mmol/L (Wiggam, O'Kane et al. 1997) oppure se il rapporto molare tra il glucosio e il β-idrossibutirrato ematici è uguale o minore di 1 (Meidenbauer, Mukherjee et al. 2015). Dato che i chetoni acetoacetato e β-idrossibutirrato sono acidi, lo stato di chetosi implica una condizione di acidosi. Siccome il pH del sangue è 7,4 e la pKa dell’acetoacetato è 3,8 e quella del β-idrossibutirrato è 4,8, questi acidi circolano nel sangue in forma dissociata e sono eliminati insieme agli ioni sodio e potassio (Siliprandi & Tettamanti 2011) . Questa perdita di cationi porta una diminuzione del pH che viene normalmente tamponata dal corpo tranne quando l’assunzione di sodio e potassio è impedita (Phinney 2004) oppure in caso di diabete scompensato, quando c’è una sovrapproduzione di corpi chetonici con livelli superiori a 20 mmol/L e conseguente riduzione del pH. Il biochimico Hans Krebs fu il primo a distinguere la chetosi fisiologica da quella patologica (Krebs 1966). Per i muscoli scheletrici e cardiaco, che utilizzano normalmente i grassi, l’utilizzo dei corpi chetonici a scopo energetico è un vantaggio relativo, mentre per il sistema nervoso centrale, in cui l’accesso degli acidi grassi è impedito dalla barriera ematoencefalica, la disponibilità dei corpi chetonici è un importante surrogato del glucosio, che è il substrato abituale dei neuroni. Durante il digiuno, in dieta chetogenica e nei neonati, il cervello utilizza i corpi chetonici come combustibili principali al posto del glucosio (Laeger, Metges et al. 2010), proporzionalmente al grado di chetosi (Hartman, Gasior et al.). Il β-idrossibutirrato è il principale corpo chetonico circolante e il suo trasporto attraverso la barriera ematoencefalica avviene sia mediante diffusione che attraverso i trasportatori MCT1 e MCT2, dei quali i primi aumentano durante una dieta chetogenica (Newman, Verdin 2014). Quest’azione complementare tra il fegato, che produce i corpi chetonici in assenza di carboidrati, e il sistema nervoso centrale che li può utilizzare, è un evento molto importante che fu determinante per la sopravvivenza della specie umana nei millenni.

La mia ricerca si è focalizzata su tre importanti aspetti delle diete chetogeniche - connesse alla perdita di peso - che richiedevano di essere approfonditi:
1. il mantenimento del peso perso dopo una dieta chetogenica: il mantenimento del peso perso a lungo nel tempo è impegnativo e la paura di ritornare velocemente al peso iniziale è comune, tanto che questo fenomeno viene chiamato “effetto yo-yo". A questo proposito, le diete a basso contenuto di carboidrati sono note per portare risultati migliori rispetto alle diete a basso contenuto di grassi in termini di perdita di peso (Shai, Schwarzfuchs et al. 2008c), ma non di “compliance” (adesione al protocollo) (Greenberg, Stampfer et al. 2009). Recentemente, Sumithran e collaboratori hanno dimostrato che l'aumento dei livelli circolanti di grelina e del livello di appetito tipici di una dieta ipocalorica erano minori durante un protocollo chetogenico (Sumithran, Prendergast et al. 2013). Abbiamo quindi ipotizzato che alcuni aspetti della dieta chetogenica come il mantenimento della massa muscolare, del metabolismo energetico basale e la stabilità del principale ormone oressigenico (grelina) combinati con gli effetti benefici della nutrizione tradizionale mediterranea, potessero favorire la perdita di peso a lungo nel tempo. Lo scopo del nostro studio è stato quindi quello di indagare l'effetto sul peso e sulla composizione corporea di due brevi periodi di una dieta chetogenica modificata, cioè una dieta fitochetogenica mediterranea (KEMEPHY) (Paoli, Cenci et al. 2010a, Paoli 2011, Paoli 2012) intervallata da 2 periodi più lunghi di dieta di mantenimento basata sulla dieta mediterranea tradizionale per un periodo totale di 12 mesi. I soggetti reclutati erano obesi o in sovrappeso e lo studio è stato retrospettivo. Abbiamo analizzato 89 soggetti (uomini e donne) di età compresa tra i 25 e i 65 anni che erano in uno stato di buona salute generale benchè fossero obesi (IMC medio 35.82 ± 4.11 kg/m2). I risultati di questo studio hanno dimostrato che la maggioranza dei soggetti ha ottenuto una significativa perdita di peso (10%) a seguito delle due fasi di dieta chetogenica e l’aderenza al protocollo è stata alta sia durante i sei mesi di perdita di peso sia nei successivi sei mesi di mantenimento, senza riacquisto del peso. Inoltre, il protocollo proposto ha portato miglioramenti nella maggior parte dei soggetti dei livelli di parametri importanti per la salute (colesterolo totale, colesterolo LDL, trigliceridi e livelli di glucosio). L’alta “compliance” è stato un fattore determinante per i risultati ottenuti;
2. la formulazione di nuovi prodotti a basso contenuto di carboidrati per sopperire alla mancanza del sapore dolce durante una dieta chetogenica: un aspetto delle diete chetogeniche difficile da tollerare nel lungo tempo, soprattutto per chi ha una spiccata preferenza per i dolci, è la mancanza di questo sapore. In dieta chetogenica è necessario mantenere un basso livello di glicemia (circa 80-90 mg/dL) per evitare i picchi di insulina (Paoli, Canato et al. 2011) e permettere così ai soggetti di migliorare l'ossidazione dei grassi come dimostrato da Paoli et al. (Paoli, Grimaldi et al. 2012) e da Tagliabue et al. (Tagliabue, Bertoli et al. 2012). Oggi la nuova tecnologia alimentare, che è in grado di costruire prodotti ultra-processati con un contenuto di zucchero molto basso e un alto contenuto di proteine e fibre, può aiutare a risolvere questo problema, formulando prodotti di elevata appetibilità in un formato pronto per il consumo, utili sia in chetosi che in diete ipoglucidiche più moderate. Di solito i prodotti ultra-processati mancano di proteine e fibre e producono picchi post-prandiali di glucosio e insulina (OPS WHO 2015) . Questo effetto provoca un forte desiderio di cibo con una preferenza per i carboidrati ad alto indice glicemico (Lennerz, Alsop et al. 2013), fenomeno definito come "carb-craving" (Ventura, Santander et al. 2014). Al fine di analizzare l'effetto di 10 diversi alimenti ultra-processati ad alto contenuto proteico e basso contento di carboidrati sulla glicemia, abbiamo reclutato 14 donne sane e abbiamo testato la loro risposta glicemica attraverso il metodo del punteggio glicemico (“glucose-score”, GS). Tutti gli alimenti testati hanno prodotto, rispetto al glucosio, una risposta glicemica significativamente inferiore e il loro GS è risultato inferiore a 25 (rispetto al valore di riferimento del GS del glucosio che è 100). Abbiamo quindi concluso che la riformulazione di prodotti ultra-processati pronti al consumo in una versione ad alto contenuto proteico e basso contenuto di carboidrati è in grado di produrre una risposta glicemica significativamente più bassa, pur mantenendo l'alto valore del pratico formato pronto per l'uso e l'alta appetibilità richiesta dai consumatori, facilitando quindi l'adesione a una dieta chetogenica di individui che tendono ad avere una forte preferenza per i cibi dolci;
3. l’effetto delle diete chetogeniche sulle funzioni cognitive: il range di variazione della glicemia o dei corpi chetonici nel sangue di soggetti non diabetici è ampia e ciascuno di essi può essere utilizzato come energia dal cervello. I dati sugli effetti della variazione dei livelli di glicemia e chetonemia sulle funzioni cognitive di esseri umani sani dopo diversi tipi di dieta sono scarsi. Lo scopo di questo studio è stato confrontare gli effetti della variazione di glicemia e chetonemia dopo dieci giorni di due differenti diete chetogeniche e di una dieta mediterranea ipocalorica (MD) sulla memoria di lavoro e sulle funzioni esecutive in 63 giovani donne sovrappeso, sedentarie e in buona salute (IMC> 25, età: 20-35) che sono state reclutate nella zona universitaria. I soggetti sono stati divisi in gruppi in base al giorno di inizio della loro fase follicolare per minimizzare gli effetti ormonali sull'umore e le misurazioni basali sono state effettuate cinque giorni prima dell'inizio del protocollo dietetico. I seguenti controlli sono stati fissati al giorno di inizio della dieta (t1), al terzo (t3), al quinto (t5), al settimo (t7) e all'ultimo giorno (t10). Al controllo iniziale è stato misurato il peso dei soggetti ed è stata eseguita un'analisi impedenziometrica. I soggetti hanno poi assunto una colazione ad alto contenuto di carboidrati e hanno completato i test psicologici. Al t1, T3, T5, T7 e t10 sono stati misurati il livello dei corpi chetonici e la glicemia, così come i livelli di appetito. Nel giorno dell'ultimo controllo (T10) i soggetti hanno ripetuto l'analisi impedenziometrica, la misura del peso corporeo e, dopo la colazione (ogni gruppo ha assunto una colazione diversa a seconda della dieta prescritta), hanno completato i test psicologici. I test psicologici consistevano in un test sull'umore, due compiti cognitivi, uno per indagare la memoria di lavoro (“visuo-spatial n back”) e uno per analizzare le funzioni esecutive (“inhibitory control task”) e in una scala VAS per testare il livello di appetito. 45 soggetti hanno completato lo studio. Considerando tutti i partecipanti insieme, i livelli di glucosio pre-dieta correlavano positivamente con il tempo di reazione nel “go-trial” del test delle funzioni esecutive (r(43) = 0,358, p = 0,018), ma questa relazione non è stata trovata nel post-dieta, sia quando i soggetti sono stati analizzati tutti insieme che quando i soggetti sono stati divisi in base al tipo di dieta seguita. Nello stesso test psicologico, nel post-dieta la misura della chetonemia ha mostrato una correlazione negativa con l'accuratezza ai compiti “no-go” (r(29) = -0,455, p = 0,027). Possiamo quindi concludere che giovani soggetti in sovrappeso con livelli di glicemia inferiori al livello di pre-diabete sono stati influenzati negativamente da una colazione ad alto contenuto di carboidrati nel corso di un test di funzioni esecutive. Inoltre, l'effetto di moderati livelli di corpi chetonici (2 ± 1,3 mmol / L) ha nfluenzato negativamente l'accuratezza nelle prove “no-go” del test sulle funzioni esecutive.

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EPrint type:Ph.D. thesis
Tutor:Paoli, Antonio
Ph.D. course:Ciclo 28 > Scuole 28 > BIOSCIENZE E BIOTECNOLOGIE > NEUROBIOLOGIA
Data di deposito della tesi:28 January 2017
Anno di Pubblicazione:27 January 2017
Key Words:dieta chetogenica/dieta mediterranea/ dimagrimento / alimenti ultraprocessati/ dieta e funzioni cognitive/ ketogenic diet/mediterranean diet/ weight loss / ultraprocessed foods / diet and cognitive functions
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/09 Fisiologia
Struttura di riferimento:Dipartimenti > Dipartimento di Biologia
Codice ID:10010
Depositato il:06 Nov 2017 14:03
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