Chronotype

Chronotype is a subject's attitude to carry out most of their daily activities in the first part (morning chronotype or ‘lark’) or in the second part (evening chronotype or ‘owl’) of the day^{(Reference Roenneberg, Kuehnle and Juda13)}. Based on circadian behavioural phenotype variants, three categories of chronotypes could be identified: morning, evening and intermediate chronotypes. The morning chronotype prefers to wake up early and do their daily activities in the first half of the day. The evening chronotype prefers to wake up later in the morning and do most of their daily activities in the afternoon or evening. In an intermediate position between these two categories, there is an intermediate chronotype, who has habits that fall between morning and evening chronotypes without a clear preference between morning and evening^{(Reference Roenneberg, Kuehnle and Juda13)}.

The nutritional habit of evening chronotype is usually unhealthy and is characterised by delayed mealtimes, most of the daily food intake in the second half of the day and skipping breakfast^{(Reference Mazri, Manaf and Shahar14,Reference van der Merwe, Munch and Kruger15)} . In particular, we previously demonstrated in a cross-sectional study aiming to investigate the association between chronotype categories (morning, evening, intermediate) and adherence to Mediterranean diet in 172 middle-aged Italian adults, that evening chronotype showed the lowest adherence to Mediterranean diet compared to morning and intermediate chronotypes^{(Reference Muscogiuri, Barrea and Aprano16)}. Given the role of the association of diet with chronotype we also suggested a specific cut-off of the Prevención con Dieta Mediterránea score, a validated questionnaire for assessing adherence to Mediterranean diet, which identifies subjects with the evening chronotype^{(Reference Barrea, Muscogiuri and Savastano17)}. Of note, a Prevención con Dieta Mediterránea score <8 was the threshold for identifying subjects with the evening chronotype^{(Reference Barrea, Muscogiuri and Savastano17)}.

Almost all studies examining the aspect of mealtimes reported similar results, with earlier chronotypes having earlier mealtimes and later chronotypes having later mealtimes^{(Reference Munoz, Canavate and Hernandez18–Reference Teixeira, Mota and Crispim21)}. Thus, these results reflect the possibility that the norm of mealtime follows a person's own biological clock despite social clock limitations. Meule et al. suggested that the biochemical rhythm of appetite-regulating peptides (leptin and ghrelin) might underlie this behaviour, since the evening chronotype has a delayed release of ghrelin and leptin than the morning chronotype^{(Reference Meule, Roeser and Randler22)}. The results of recent research have added to the growing body of evidence supporting the link between chronotype and breakfast^{(Reference Teixeira, Mota and Crispim21–Reference Lopez-Minguez, Dashti and Madrid-Valero23)}. A genetic study was conducted on fifty-three pairs of female twins to investigate the influence of genetic inheritance on mealtimes^{(Reference Lopez-Minguez, Dashti and Madrid-Valero23)}. They found that the time of breakfast (56 %) and lunch (38 %) was mainly genetically influenced, but not the time of dinner. In addition, the genetic heritability of waking time was also greater than sleeping time (55 v. 38 %)^{(Reference Lopez-Minguez, Dashti and Madrid-Valero23)}. Hence, this could be the possible underlying mechanism behind the relationship between chronotype and breakfast habits, since chronotype was also associated with sleep–wake time^{(Reference Sato-Mito, Sasaki and Murakami24,Reference Sato-Mito, Shibata and Sasaki25)} . Another interesting finding from the latest research is that only the morning chronotype benefited from higher energy intake earlier in the day (within 2 h of waking) and was protected from obesity, with a reduced likelihood of developing overweight or obesity^{(Reference Xiao, Garaulet and Scheer26)}. Although many studies highlight the importance of breakfast^{(Reference Jakubowicz, Wainstein and Landau27,Reference Yasuda, Asako and Arimitsu28)} , not everyone (especially the evening chronotype) may be able to reap its benefits. There are a limited number of studies on the effects of delaying meal timing in individuals with evening chronotypes. Delay in eating dinner or supper was less severe in evening chronotypes than in shift workers (range: 7:19 p.m. to 9:31 p.m.)^{(Reference Mazri, Manaf and Shahar14)}. Nonetheless, evening chronotypes remain subject to a milder form of chronodisruption (in terms of irregular and delayed mealtimes)^{(Reference Anothaisintawee, Lertrattananon and Thamakaison29)}. The subjects belonging to different chronotype categories mostly differ in feeding timing, although they reported similar nutrient intake^{(Reference Mazri, Manaf and Shahar14,Reference van der Merwe, Munch and Kruger15,Reference Maukonen, Kanerva and Partonen30)} . Indeed, it has been reported that subjects with evening chronotype were more prone to have less energy intake by 4–5 % in the morning and more energy intake by 6–7 % at evening compared to subjects with morning chronotype^{(Reference Maukonen, Kanerva and Partonen30)}. Thus, it highlights that although subjects belonging to different chronotype categories have the same amount of energy intake during the day, the breakdown of energy intake throughout the day is different. In addition, subjects with morning chronotype prefer to eat protein-rich meal in the first half of the day while subjects with evening chronotype prefer sucrose intake^{(Reference Xiao, Garaulet and Scheer26)}. The preference to consume more alcohol and caffeine is another feature of subjects with evening chronotype^{(Reference Whittier, Sanchez and Castaneda31)} that can also contribute to the higher prevalence sleep disturbances in this category of subjects^{(Reference Clark and Landolt32,Reference Ebrahim, Shapiro and Williams33)} .

Among the several nutritional aspects addressed so far, it appears that chronotype also influences eating speed. In order to better characterise the eating habits of subjects with obesity belonging to three different chronotype categories, we previously investigated eating speed during the three main meals in eighty-one subjects with overweight/obesity in a cross-sectional study^{(Reference Verde, Docimo and Chirico34)}. To investigate the duration of main meals, a dietary interview by a qualified nutritionist was conducted. Subjects with the evening chronotype spent significantly less time on lunch than subjects with the morning chronotype^{(Reference Verde, Docimo and Chirico34)}.

Consequently, the nutritional habits of subjects with evening chronotype increase the risk of developing obesity and obesity-related disease.

In this regard, chronotype seems to be also involved in metabolic comorbidities. Results of our previous research in 174 middle-aged Italian adults found out that the evening chronotype was linked to an increased risk of type 2 diabetes and CVD compared to morning chronotype after adjustment for sex, BMI, sleep quality and adherence to Mediterranean diet^{(Reference Muscogiuri, Barrea and Aprano35)}. In a cross-sectional study in eighty-seven subjects with obesity aimed to investigate the association of non-alcoholic fatty liver diseases with chronotype categories, only individuals with the evening chronotype were above the threshold of non-alcoholic steatohepatitis evaluated as index of non-alcoholic steatohepatitis (≥50)^{(Reference Vetrani, Barrea and Verde36)}. In addition, subjects with the evening chronotype presented significantly higher indirect indices of non-alcoholic fatty liver diseases such as visceral adipose index, liver fatty equation, hepatic steatosis index and index of non-alcoholic steatohepatitis than morning chronotype, also after the adjustment for age, sex and BMI^{(Reference Vetrani, Barrea and Verde36)}.

Besides as seen earlier a role in the development of metabolic comorbidities and in determining eating habits in obesity, chronotype also appears to influence the efficacy of nutritional approaches for obesity. In particular, existing literature suggests that very low-energy ketogenic diet can be an effective intervention for weight loss and improving metabolic health in individuals with obesity^{(Reference Barrea, Verde and Schiavo37–Reference Muscogiuri, El Ghoch and Colao39)}. In this regard, we carried out a study to investigate whether chronotype categories can have a role in determining the efficacy of very low-energy ketogenic diet in terms of weight loss and changes of body composition in 248 women with overweight or obesity^{(Reference Verde, Barrea and Docimo40)}. Women with evening chronotype experienced significantly less weight loss, reduced fat mass and increased fat-free mass than women with morning chronotype. Using a linear regression model, chronotype score was the main predictor of weight loss achieved with very low-energy ketogenic diet^{(Reference Verde, Barrea and Docimo40)}.

In conclusion, the circadian preference towards eveningness is associated with a delay in meal timing, the breakfast skipping habit, engagement with excessive consumption during night-time, lower protein and vegetables intake, as well as increased sucrose, sweets, caffeine and alcohol intake. A limited number of studies have also shown that the aforementioned chronotype was related to a lower intake of grains and fruits. Despite that, both morning and evening chronotypes relatively consumed the same number of energy, amount of carbohydrates, fat, cholesterol, fibre, legumes, meat, fish and dairy products. Nonetheless, more aspects of dietary behaviours, micronutrients and other food group intakes between chronotypes remain uncertain, and more studies are required to elucidate the relationship between chronotype and body weight in the long term.

Eating speed

Eating speed is the length of time spent eating. In particular it has been highlighted that lower energy intake is usually accompanied by slow-eating speed thus providing important evidence that slow eating is a fundamental component of healthy dietary pattern^{(Reference Ohkuma, Hirakawa and Nakamura41)}. In addition, eating speed is of paramount importance because if it is too fast, it increases the risk of developing obesity and obesity-related cardiometabolic diseases^{(Reference Ohkuma, Hirakawa and Nakamura41,Reference Barrea, Vetrani and Verde42)} . This is due to the impact of eating speed on secretion of hormones that play a role in the regulation of satiety and appetite^{(Reference Kokkinos, le Roux and Alexiadou43)}. In fact, slow-eating speed results in an increase in the secretion of peptide YY and glucagon-like peptide-1, that in turn exert a beneficial effect on weight^{(Reference Kokkinos, le Roux and Alexiadou43)}. Eating speed is determined by mastication that could also have an impact on energy intake and body weight because it could modify the composition of the bolus thus making it more digestible andg havin a different effect on secretion of satiety and appetite hormones^{(Reference Kokkinos, le Roux and Alexiadou43)}.

It is interesting to underline that eating speed could also have a role in determining the risk of developing obesity-related cardiometabolic complications^{(Reference Barrea, Vetrani and Verde42,Reference Paz-Graniel, Babio and Mendez44–Reference Tao, Yang and Huang46)} . However, in the assessment of patients with obesity, eating speed is not usually evaluated, just giving importance to BMI, waist circumference, waist:hip ratio and waist:height ratio, currently considered the main markers of health risk in obesity^{(Reference Yumuk, Tsigos and Fried8)}. These parameters reflect the unhealthy long-term behaviours in the body^{(Reference Phelan, Halfman and Pinto47,Reference Teixeira and Marques48)} . In this context, eating speed might become an early marker that could predict long-term nutritional behaviours. Indeed, eating speed has been used in several Japanese cohort studies as a predictive factor for obesity^{(Reference Sakurai, Nakamura and Miura45,Reference Kudo, Asahi and Satoh49–Reference Ochiai, Shirasawa and Nanri51)} . However, in most of the studies carried out on obesity, especially outside of Asia, eating speed is often not taken into account, thus missing important information on nutritional habits. Thus, it would be of paramount importance to include eating speed in the assessment of patients with obesity because acting on this parameter could contribute to implement the efficacy of current anti-obesity treatments and in subjects at high risk to develop weight excess, it could contribute to prevent obesity.

Eating speed has not only been associated with obesity. Indeed, a cross-sectional study has been carried out aiming to investigate the link between eating speed and cardiovascular risk factors in 792 subjects previously enrolled in the Prevención con Dieta Mediterránea study^{(Reference Paz-Graniel, Babio and Mendez44)}. Each subject self-reported eating speed thus was then categorised as slow, medium or fast. The main finding of this study was that fast-eating subjects had 59 % more chances to develop hypertriglyceridaemia compared to slow-eating subjects, also after adjustment for potential confounders^{(Reference Paz-Graniel, Babio and Mendez44)}. We also carried out a similar cross-sectional study in eighty-seven subjects with obesity aimed to investigate the effect of eating speed at the main meals (breakfast, lunch and dinner) on the risk of developing cardiometabolic diseases (type 2 diabetes mellitus, dyslipidaemia and hypertension)^{(Reference Barrea, Vetrani and Verde42)}. A dietary interview was performed to collect information about meal duration and eating habits at the main meals. According to median value of meal duration, meals were classified into two groups: fast-eating group and slow-eating group. Of note, the prevalence of dyslipidaemia was more than twice in the fast-eating group compared to the slow-eating group at lunch and dinner. Fast-eating group had a significantly higher risk of dyslipidaemia than the slow-eating group at lunch and dinner^{(Reference Barrea, Vetrani and Verde42)}. Another interesting study carried out in the Netherlands aimed to evaluate what was the association of eating speed with consumed foods and the macronutrient composition of nutritional pattern^{(Reference Viskaal-van Dongen, Kok and de Graaf52)}. The authors found that eating speed was positively correlated with food and energy intake. In addition, eating speed was inversely correlated with energy density and positively with water content. The intake of carbohydrate, protein and fibre content was the greater the faster eating rate was, thus suggesting that an overconsumption of food may occur when subjects tend to eat fast^{(Reference Viskaal-van Dongen, Kok and de Graaf52)}. Visceral adipose tissue is considered a key risk factor for obesity-related cardiometabolic diseases^{(Reference Neeland, Ross and Despres2)}. Japanese researchers aimed to evaluate the association of eating speed with fat deposition in subjects without obesity^{(Reference Iwasaki, Hirose and Azuma53)}. They enrolled 381 participants undergoing MRI in order to quantify visceral and subcutaneous fat areas. Eating speed was self-reported by each subject filling a questionnaire. Interestingly, the prevalence of visceral adipose tissue ≥100 cm² was higher in fast eaters compared to slow eaters while no difference in subcutaneous adipose tissue was detected between the two groups. Finally, they found that eating speed was positively correlated with visceral adipose tissue, while this association was not found with subcutaneous adipose tissue^{(Reference Iwasaki, Hirose and Azuma53)}.

It is well known that among factors that influence the predisposition to develop obesity, physical activity plays an important role and it should be taken into account as confounding factors in studies carried out in subjects with obesity^{(Reference Hankinson, Daviglus and Bouchard54)}. Interestingly, eating speed is associated with the risk of developing obesity, also after adjustment for physical activity as demonstrated in several studies^{(Reference Nagahama, Kurotani and Pham55–Reference Tanihara, Imatoh and Miyazaki57)}. Although a strong relationship has been highlighted in the earlier reported evidence between obesity and eating speed, the cross-sectional design of these studies does not allow drawing conclusion on casual association. More information was provided on that sense by a longitudinal study that was carried out aiming to investigate the effects of changes in lifestyle habits on changes in obesity, mostly focusing on eating speed and type 2 diabetes, using health checkup and insurance claims data that were generated from 2008 to 2013^{(Reference Hurst and Fukuda58)}. Data coming from 59 717 subjects that were diagnosed with type 2 diabetes in the study period were analysed. Also eating speed, BMI and lifestyle habits (eating dinner within 2 h of sleeping, after-dinner snacking, skipping breakfast, alcohol consumption frequency, sleep adequacy and tobacco consumption) were assessed. Slow eating was associated with a decreased risk of developing obesity; indeed, slow eaters had lower BMI and waist circumference than fast eaters thus suggesting that interventions focused on slowdown of eating speed may be a promising approach to prevent obesity^{(Reference Hurst and Fukuda58)}. Another longitudinal study was carried out to investigate the association of eating speed with obesity in 529 male workers receiving health checkups in 2000 and 2008^{(Reference Tanihara, Imatoh and Miyazaki57)}. In 2008, information on alcohol consumption, smoking status, self-reported speed of eating and exercise was collected while height and weight were assessed in both 2000 and 2008. Interestingly, fast eaters experienced a higher weight gain (1⋅9 kg) compared to slow eaters (0⋅7 kg). Although the statistical significance was detected in the 20–29 year age group, a trend was detected also in other age groups, thus suggesting that the rate of weight gain was tightly related to eating speed^{(Reference Tanihara, Imatoh and Miyazaki57)}.

Also, a sex difference has been detected in eating speed^{(Reference Nanri, Miyaji and Kochi50,Reference Iwasaki, Hirose and Azuma53,Reference Hurst and Fukuda58)} . Indeed, males are more commonly fast eaters than females^{(Reference Nanri, Miyaji and Kochi50,Reference Iwasaki, Hirose and Azuma53,Reference Hurst and Fukuda58)} and this could partially explain also the increased risk of developing obesity found in this sex^{(Reference Cooper, Gupta and Moustafa59)}.

Eating speed has been also reported to be associated with metabolic syndrome^{(Reference Nanri, Miyaji and Kochi50,Reference Nagahama, Kurotani and Pham55,Reference Zhu, Haruyama and Muto60)} . Indeed, a study carried out in Japan in 8941 community residents from Soka city in Saitama prefecture, participating in a baseline survey in 2008 and followed up until 2011 aimed to investigate the association between eating speed and incidence of metabolic syndrome using Cox proportional hazards models adjusted for potential confounding variables^{(Reference Zhu, Haruyama and Muto60)}. During the 3-year follow-up, 647 subjects developed metabolic syndrome (25⋅0 cases/1000 person-years). In particular, the incidence rates of metabolic syndrome were higher in fast eaters (3⋅1 %) than slow eaters (2⋅3 %). Eating speed was significantly associated with waist circumference and HDL-cholesterol components of metabolic risk factors. These results suggested that targeting eating speed could be an additional tool to prevent metabolic syndrome^{(Reference Zhu, Haruyama and Muto60)}. Similar results were found in another cross-sectional study carried out in Japan in 56 865 subjects (41 820 males and 15 045 females) without history of CVD that attended a health checkup in 2011 investigating the association between self-reported eating rate and metabolic syndrome^{(Reference Nagahama, Kurotani and Pham55)}. The main findings of this study were that eating speed was significantly and positively associated with metabolic syndrome and with abdominal obesity. The link of eating speed and metabolic syndrome and its components was attenuated after adjustment for BMI; however, the link between slow-eating speed and lower odds of hypertension and impaired glycaemia as well as the link between fast-eating speed and higher odds of dyslipidaemia remained significant also after adjustment for confounding factors^{(Reference Nagahama, Kurotani and Pham55)}. Evidence on the association between eating speed and metabolic syndrome comes also from a prospective study carried out in a Japanese working population^{(Reference Nanri, Miyaji and Kochi50)}. One thousand and eighteen workers without metabolic syndrome at baseline were enrolled and were assessed at baseline and after 3 years. Eating speed was self-reported and metabolic syndrome was diagnosed according to criteria joint from several international societies. The relevant results of this study were that fast eaters had an increased odds of developing metabolic syndrome compared with medium eaters thus suggesting that eating speed was associated with a risk of developing metabolic syndrome that was independent from BMI, BMI change between baseline and follow up surveys and total energy intake^{(Reference Nanri, Miyaji and Kochi50)}.

Beyond the association of eating speed with metabolic syndrome, it has been reported also a link with metabolic parameters^{(Reference Tao, Yang and Huang46)}. A cross-sectional study carried out in 7972 Chinese adults found that eating speed was significantly associated with a high risk of hypertension and visceral obesity for both sexes^{(Reference Tao, Yang and Huang46)}. In addition, eating speed was linked with a high risk of hypertriglyceridaemia and low HDL-cholesterol levels in males while it was associated with alterations of fasting plasma glucose in females^{(Reference Tao, Yang and Huang46)}.

Little is known regarding the role of eating speed in the context of diabetes; a study carried out in 5479 Japanese adults with HbA1c <6⋅5 % participating in health checks investigated the relationship between eating behaviour and poor glycaemic control^{(Reference Iwasaki, Hirose and Azuma53)}. A survey was conducted in 2013 and the very same subjects that participated in this survey were subsequently followed up until 2017. Poor glycaemic control was defined as HbA1c ≥ 6⋅5 % or increases in HbA1c of ≥0⋅5 % and/or taking antidiabetic medications. This study found that fast eaters, mostly if they skipped breakfast ≥3 times/week were at high risk of having poor glycaemic control and obesity^{(Reference Iwasaki, Hirose and Azuma53)}. Also in Japan, a study investigated the effect of eating speed on the risk of new onset of type 2 diabetes^{(Reference Kudo, Asahi and Satoh49)}. Data coming from the nation-wide annual health check programme in Japan examined 197 825 participants without diabetes in 2008, that were followed up for 3 years. Interestingly, the prevalence of fast eaters, subjects snacking after supper and/or before sleep and/or skipping breakfast was higher in the new-onset diabetes group than in the group not developing diabetes mellitus. Eating speed was confirmed to be a risk factor for the development of diabetes also after adjustment for confounding factors^{(Reference Kudo, Asahi and Satoh49)}.

The earlier reported evidence suggests that eating speed could play an important role in determining the risk of developing obesity and obesity-related cardiometabolic diseases. However, most of these studies were cross-sectional and further studies, mostly intervention ones, need to be carried out in order to confirm the causal association between eating speed and metabolic diseases. Another issue that should be overcome is the assessment of eating speed that being self-reported, most of the time could not be reliable. Thus, the set-up of a validated tool to assess eating speed is mandatory. If a causal role of eating speed in the context of metabolic diseases would be confirmed, it could be useful to include eating speed in the assessment of subjects with obesity in order to identify those at high risk of cardiometabolic diseases and to establish tailored intervention to slowdown eating speed.