The effects of whole milk compared to skim milk and apple juice consumption in breakfast on appetite and energy intake in obese children: a three-way randomized crossover clinical trial

Obesity has become a global concern especially among children [1]. According to the reports provided by world health organization (WHO) in 2010, it is assumed that around 43 million children experienced obesity and more than twice this population were exposed to overweight all around the world [1]. Kelishadi et al. showed that obesity is affecting 8.8% of Iranian children based on the criteria explained by Center for Disease Control (CDC) [2]. Childhood obesity is of great importance because several investigations have provided evidence that there is a direct relationship between childhood obesity and chronic non-communicable diseases such as diabetes mellitus, cardiovascular diseases, and depression in later life [3].

Several strategies have been introduced for controlling the appetite, and energy intake for the management of body weight [4]. In particular, the approaches to control satiety and energy intake are important for children with obesity, as the low-calorie diets are not recommended for this age group because of their possible adverse effect on growth [5]. Although the studies have led to inconsistent results, a number of publications have suggested that milk and dairy products intake may reduce appetite and short-term energy intake [6]. For instance, a study done by Mehrabani et al. on 34 boys with obesity showed that drinking low-fat milk causes a significant decrease in appetite and energy intake at launch when compared with water and apple juice as the iso-volumic and iso-volumic/iso-energetic control beverages, respectively [7]. On the other hand, another study showed that increasing the dairy consumption from one portion per day to 3 does not affect appetite and may lead to increased energy intake and consequently weight gain [8]. In another study, the effect of receiving orange juice, 1% milk fat and cola in comparison with water on hunger, satiety and energy intake in the next meal was studied. All of these beverages increased the satiety and reduced starvation rates compared to water [9].

The effect of dairy on satiety is attributed to several components such as protein, lactose, and lipids including linoleic acid and conjugated fatty acids. However, it is not clear that which component is responsible for the effect [10]. Researchers have suggested that proteins might play a strong role in controlling appetite. The effect of proteins in the short term regulation of the food intake is related to the increased plasma concentration of peptide hormones in the gastrointestinal tract, which reduces gastric emptying, gastrointestinal movements and appetite [10]. Furthermore, the fat content of dairy is also proposed to have a role in reducing appetite [10]. The mechanism through which the fat compartment of dairy affects satiety is not well understood; however, studies have shown that the type and the structure of fatty acids, their chain length, and degree of saturation play an essential role in appetite [11]. It has been shown that fat can prolong the passage of food from the gastrointestinal tract and stimulate the release of peptide YY (PYY), cholecystokinin, glucagon-like peptides, and suppresses appetite and energy intake [12].

While studies have come to controversial results regarding the effect of dairy consumption on satiety in children, we are not aware of any study trying to examine the appetite lowering effect of dairy fat. Therefore, in the present study, we aimed to assess the effect of consuming skim milk compared to full-fat milk and apple juice in breakfast on appetite and short-term energy intake in children with obesity through a three-way randomized cross-over clinical trial. We compared the skim milk with the full-fat milk to see the possible effect of fat content of dairy on appetite and energy intake at lunch. Apple juice was also selected as the control beverage to see if the skim milk lowers the satiety when compared to an iso-volumic/iso-energetic beverage.

About 140 children were initially assessed for inclusion criteria. Fifty children did not meet the criteria and the parents of 40 parents declined the invitation for the first meeting which was arranged for describing the objectives of the study. Parents of 50 children gave the informed consent and their children entered into the study. However, one boy and one girl refused to continue the study after the first study period. Therefore, 48 children (24 girls and 24 boys were included in the present study) completed the study and included in the analyses. The study flow diagram is shown in Fig. 1.

The effect of beverages on appetite

All the analyses for the comparison of mean appetite and its components scores were adjusted for gender, age, BMI, and rolling method. The total appetite score and its components were significantly changed by time for all intervention beverages in all participants as well as either gender (P < 0.05). The analysis of the total appetite scores in the total population revealed that the appetite was significantly lower in the whole milk period compared to skim milk before eating the breakfast (P < 0.05). Furthermore, the mean satiety level was significantly higher in the whole milk period compared to the skim milk period at 11:30 a.m. (P < 0.05). The intervention beverages were not statistically different regarding their effect on appetite in other testing occasions (Fig. 2).

The comparison between the effects of intervention beverages on different appetite components in all participants are provided in Fig. 3. The desire to eat was significantly higher before consumption of the breakfast containing apple juice compared to whole milk (P < 0.05); furthermore, the sense of fullness was significantly higher before breakfast in the whole milk period compare to skim milk period (P < 0.05). It was shown that the level of Hunger and prospective consumption of food was significantly lower at 11:30 a.m. when participants consumed whole milk at breakfast compared to skim milk (P < 0.05).

The gender-specific effect of intervention beverages on the overall appetite and its components are provided in Additional file 1. The mean appetite score was lower right after breakfast consumption (7:30 a.m.) in male participants when they consumed apple juice with their breakfast compared to whole milk (P < 0.05). There was no difference between beverages in other testing occasions when the analysis was done in male participants (Additional file 1: Figure S1). The male participants felt higher levels of fullness before eating breakfast with whole milk when compared to skim milk (P < 0.05). However, the sense of hunger was significantly higher right after breakfast after drinking the whole milk compared to apple juice (P < 0.05) (Additional file 1: Figure S2).

The appetite score was significantly lower before drinking the whole milk with breakfast compared to skim milk in girls (P < 0.05). At 9:30 a.m. (T3) the appetite score was significantly higher after drinking the apple juice compared to skim milk in females (P < 0.05); furthermore, the appetite was significantly lower at 11:30 a.m. (T5) after drinking the whole milk compared to skim milk (P < 0.05) (Additional file 1: Figure S3). The same associations were found for the desire to eat in the female participants (Additional file 1: Figure S4). Moreover, the sense of fullness was significantly higher at 9:30 a.m. in females when the skim milk was compare to apple juice (P < 0.05). It is also revealed that the sense of prospective consumption was significantly higher after drinking the skim milk and apple juice compared to whole milk (P < 0.05) (Additional file 1: Figure S4).

The present three-way randomized cross-over trial among children revealed that the whole milk, skim milk and apple juice does not differently affect the energy intake at lunch in either gender as well as the total population. Although the test beverages were not different in their effect on short-term energy intake, it was shown that drinking the whole milk decreases the appetite, sense of hunger and prospective consumption of food four hours after breakfast at 11:30 a.m. compared to skim milk. This finding was true in female participants but not in males. Furthermore, the appetite and sense of desire to eat were significantly lower in girls two hours (9:30 a.m.) after drinking the skim milk compared to apple juice. Previous studies have examined the effect of dairy consumption on satiety and short-term energy intake [17]. However, the different effect of full-fat milk compared to skim milk on the energy intake is not well understood. We are not aware of previous studies trying to compare dairy foods with the different fat content on the energy intake in the subsequent meal and the satiety.

The present study revealed that skim milk significantly lowers the appetite score compared to apple juice about two hours after preloads in female children but not in boys. In a study conducted by Dove et al., the consumption of skim milk, in comparison with a fruit drink, led to increased perceptions of satiety and a decreased energy intake at a subsequent meal [6]. The same effect was also shown in a study done by Mehrabani et al. [7] in which they found that low-fat milk significantly reduces the appetite and modestly decreases the short term energy intake compared to apple juice. However, the total whole day energy intake was not significantly different between the three interventions in another report by this team [18].

In the present study, we could not see the energy intake lowering effect of whole and skim milk compared to apple juice. In fact, Mehrabani et al. explored the effect of low fat milk compared to apple juice. However, the in the present study skim milk and whole milk were compared to apple juice.

Several mechanisms are suggested for the appetite lowering effect of milk intake when compared to fruit juice. Milk might exert its effect on satiety because of its high content of protein. It has been shown that proteins are more satiating in comparison with carbohydrates [19]. Changes in appetite-linked hormones, amino acids, and gluconeogenesis might be after protein consumption responsible for such an effect [20]. It is not clear that to which extent whey or casein proteins, exclusively or mixed might affect appetite. Both proteins are associated with this effect [20]. Milk also is high in lactose which is associated with reduced appetite, too. The satiating effect of lactose on energy intake, was reported to be the same as dairy protein [21]; both preloads significantly reduced the energy intake when compared with a glucose containing preload. It is also revealed that viscous beverages might have appetite lowering effect and decrease the energy intake [22]. Milk is more viscous compared with fruit drink and this may contribute to the appetite lowering effect of this beverage. Calcium which is high in dairy products might also influence appetite [23]. However, animal studies does not support this hypothesis up to now [24].

In the present study, we showed that full-fat milk significantly reduces the satiety 4 h after its drinking when compared with skim milk. The fat component of dairy products is high in conjugated linoleic acid (CLA) and medium chain triglycerides (MCTs) which their individual effect on the energy intake and subjective appetite have been proposed by a number of studies [25–27]. A study also represented that full-fat milk delays the gastric-emptying time in comparison with half-skimmed milk [28]. However, to the best of our knowledge, no study has tried to compare the skim milk and whole milk in this regard. A recent study done by Kling et al. [29] revealed that including full-fat milk in lunch decreases the amount of the lunch eaten by the children when compared with low-fat milk but the energy intake was not significantly different between the two beverages. In fact, they did not compare the effect of milk with different fat content on the satiety and energy intake in the subsequent meal. In the present study, also we found that there was no difference between skim milk and whole milk in terms of their effect on short-term energy intake; however, satiety was significantly higher four hours after consumption of whole milk compared to skim milk. In line with our result, a previous research proposed that a 4 h interval between drinking of the beverages and initiation of a test meal may reveal the effect of milk on appetite and energy intake [6]. This may explain why this effect was not significant at the other time points in the present study.

It should be noted that only children with obesity were included in the present study and the results may be different in normal weight children. Furthermore, the subsequent meal was provided five hours after drinking the test beverages and the effect may have been different if the meal was provided earlier after the intake of preloads.

In conclusion the current study revealed that providing one cup of full-fat milk, skim milk or apple juice in breakfast does not make any difference in energy intake at lunch; however, whole milk significantly reduced appetite when compared with skim milk 4 h after drinking the test beverages; which highlights the appetite-reducing effect of dairy fat. Further studies comparing the effect of full-fat versus skim milk in children exploring the effect in longer periods of time and also including normal weight participants are highly recommended.